@article {1536401, title = {Complex developmental and transcriptional dynamics underlie pollinator-driven evolutionary transitions in nectar spur morphology in Aquilegia (columbine)}, journal = {American Journal of Botany}, volume = {109}, year = {2022}, pages = {1360{\textendash}1381}, url = {https://bsapubs.onlinelibrary.wiley.com/doi/full/10.1002/ajb2.16046}, author = {Edwards, M. B. and Ballerini, E. S. and Kramer, E. M.} } @article {1429703, title = {Quantitative live imaging of floral organ initiation and floral meristem termination in Aquilegia}, journal = {Development}, volume = {149}, year = {2022}, author = {Ya Min and Stephanie Conway and Elena Kramer} } @article {1536406, title = {Genetic architecture of floral traits in bee- and hummingbird-pollinated sister species of Aquilegia (columbine)}, journal = {Evolution}, volume = {75}, year = {2021}, pages = {2197{\textendash}2216}, url = {https://academic.oup.com/evolut/article/75/9/2197/6728544}, author = {Edwards, Molly B. and Choi, Gary P. T. and Derieg, Nathan J. and Min, Ya and Diana, Angie C. and Hodges, Scott A. and Mahadevan, L. and Kramer, Elena M. and Ballerini, Evangeline S.} } @article {1536416, title = {POPOVICH, encoding a C2H2 zinc-finger transcriptionfactor, plays a central role in the development of a keyinnovation, floral nectar spurs, inAquilegia}, journal = {Proceedings of the National Academy of Science}, volume = {117}, year = {2020}, pages = {22552-22560 }, url = {https://www.pnas.org/doi/epdf/10.1073/pnas.2006912117}, author = {Ballerini, E. S. and Y. Min and M. B. Edwards and E. M. Kramer and S. A. Hodges} } @article {1323029, title = {A role for the Auxin Response Factors ARF6 and ARF8 homologs in petal spur elongation and nectary maturation in Aquilegia}, journal = {New Phytologist}, volume = {227}, year = {2020}, pages = {1392-1405}, url = {https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.16633}, author = {Zhang, R. and Min, Y. and Holappa, L. D. and C. L. Walcher-Chevillet and X. Dian and E. Donaldson and H.-Z. Kong and Kramer, E. M.} } @article {1323037, title = {Homologs of LEAFY and UNUSUAL FLORAL ORGANS promote the transition frominflorescence to floral meristem identity in the cymose Aquilegia coerulea}, journal = {Front Plant Sci}, volume = {10}, year = {2019}, pages = {1218}, author = {Sharma, B. and C. Meaders and D. Wolfe and L. Holappa and C. Walcher-Chevillet and Kramer, E. M.} } @article {1323035, title = {Comparative transcriptomics of early petal development across four diverse species of Aquilegia reveal few genes consistently associated with nectar spur development}, journal = {BMC Genomics}, volume = {20}, year = {2019}, author = {Ballerini, E. S. and Kramer, E. M. and Hodges, S. A.} } @article {1323032, title = {Developmental and molecular changes underlying the vernalization-induced transition to flowering in Aquilegia coerulea (James)}, journal = {Genes}, volume = {10}, year = {2019}, pages = {E734}, author = {Sharma, B. and T. A. Batz and R. Kaundal and Kramer, E. M. and U.R. Sanders and V. J. Mellano and N. Duhan and R. B. Larson} } @article {1323031, title = {Large-scale phylogenomic analysis suggests three ancient superclades of the WUSCHEL RELATED HOMEOBOX transcription factor family in plants}, journal = {PLoS One}, volume = {14}, year = {2019}, pages = {e0223521}, author = {Wu, C.-C. and F.W. Li and Kramer, E. M.} } @article {1140675, title = {Homologs of the STYLISH gene family control nectary development in Aquilegia}, journal = {New Phytologist}, volume = {221}, year = {2019}, pages = {1090-1100}, author = {Min, Y. and Bunn, J.I. and Kramer, E. M.} } @article {1323039, title = {The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarilypolymorphic chromosome with a unique history}, journal = {eLife}, volume = {10.7554/eLife.36426}, year = {2018}, url = {https://doi.org/10.7554/eLife.36426}, author = {Filiault, D. L. and Ballerini, E. S. and T. Mand{\'a}kov{\'a} and G. Ak{\"o}z and N. J. Derieg and J. Schmutz and J. Jenkins and J. Grimwood and S. Shu and R. D. Hayes and U. Hellsten and K. Barry and J. Yan and S. Mihaltcheva and M. Karafi{\'a}tov{\'a} and V. Nizhynska and Kramer, E. M. and M. A. Lysak and Hodges, S. A. and M. Nordborg} } @article {1323040, title = {The Aquilegia JAGGED homolog promotes proliferation of adaxial cell types in both leaves and stems}, journal = {New Phytologist}, volume = {216}, year = {2017}, pages = {536-548}, author = {Min, Y. and Kramer, E. M.} } @article {1094366, title = {Aquilegia B gene homologs promote petaloidy of the sepals and maintenance of the C domain boundary.}, journal = {EvoDevo}, volume = {8}, year = {2017}, pages = {22}, author = {Sharma, B. and Kramer, E. M.} } @article {1094356, title = {The pomegranate (Punica granatum L.) genome and the genomics of punicalagin biosynthesis.}, journal = {Plant Journal}, volume = {doi:10.1111/tpj.13625}, year = {2017}, abstract = {

Pomegranate (Punica granatum L.) is a perennial fruit crop grown since ancient times that has been planted worldwide and is known for its functional metabolites, particularly punicalagins. We have sequenced and assembled the pomegranate genome with 328 Mb anchored into nine pseudo-chromosomes and annotated 29 229 gene models. A Myrtales lineage-specific whole-genome duplication event was detected that occurred in the common ancestor before the divergence of pomegranate and Eucalyptus. Repetitive sequences accounted for 46.1\% of the assembled genome. We found that the integument development gene INNER NO OUTER (INO) was under positive selection and potentially contributed to the development of the fleshy outer layer of the seed coat, an edible part of pomegranate fruit. The genes encoding the enzymes for synthesis and degradation of lignin, hemicelluloses and cellulose were also differentially expressed between soft- and hard-seeded varieties, reflecting differences in their accumulation in cultivars differing in seed hardness. Candidate genes for punicalagin biosynthesis were identified and their expression patterns indicated that gallic acid synthesis in tissues could follow different biochemical pathways. The genome sequence of pomegranate provides a valuable resource for the dissection of many biological and biochemical traits and also provides important insights for the acceleration of breeding. Elucidation of the biochemical pathway(s) involved in punicalagin biosynthesis could assist breeding efforts to increase production of this bioactive compound.

KEYWORDS:\ \ adaption; genome; pomegranate; punicalagin biosynthesis; system evolution

}, author = {Qin, G. and C. Xu and R. Ming and H. Tang and R. Guyot and Kramer, E. M. and Hu, Y. and X. Yi and Y. Qi and X. Xu and Z. Gao and H. Pan and J. Jian and Y. Tian and Z. Yue and Xu, Y.} } @article {1094351, title = {Evolutionary analysis of Snf1-Related Protein Kinase2 (SnRK2) and Calcium Sensor (SCS) gene lineages, and dimerization of rice homologs, suggest deep biochemical conservation across angiosperms. }, journal = {Frontiers in Plant Science}, volume = {8}, year = {2017}, pages = {396}, author = {Holappa, L. D. and P.C. Ronald and Kramer, E. M.} } @article {1094346, title = {Differential expression of CYC2 genes and the elaboration of floral morphologies in Hiptage, an Old World genus of Malpighiaceae.}, journal = {International Journal of Plant Sciences}, volume = {177}, year = {2016}, pages = {551-558}, author = {Zhang, W. and Kramer, E. M. and Davis, C. C.} } @article {928206, title = {The Aquilegia JAGGED homolog promotes proliferation of adaxial cell types in both leaves and stems.}, journal = {New Phytologist}, volume = {DOI: 10.1111/nph.14282 }, year = {2016}, author = {Y Min and Kramer, E. M.} } @article {740821, title = {Stranger in a strange land: The utility and interpretation of heterologous expression}, journal = {Frontiers Plant Science}, volume = {6}, year = {2015}, pages = {734}, url = {http://journal.frontiersin.org/article/10.3389/fpls.2015.00734/full}, author = {Kramer, E. M.} } @article {591836, title = {Molecular basis for three-dimensional elaboration of the Aquilegia petal spur}, journal = {Proc Biol Sci}, volume = {282}, number = {1803}, year = {2015}, note = {

Yant, LeviCollani, SilvioPuzey, JoshuaLevy, ClaraKramer, Elena Meng1F32GM096699/GM/NIGMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2015/02/13 06:00Proc Biol Sci. 2015 Mar 22;282(1803):20142778. doi: 10.1098/rspb.2014.2778.

}, month = {Mar 22}, pages = {20142778}, abstract = {

By enforcing specific pollinator interactions, Aquilegia petal nectar spurs maintain reproductive isolation between species. Spur development is the result of three-dimensional elaboration from a comparatively two-dimensional primordium. Initiated by localized, oriented cell divisions surrounding the incipient nectary, this process creates a pouch that is extended by anisotropic cell elongation. We hypothesized that the development of this evolutionary novelty could be promoted by non-mutually exclusive factors, including (i) prolonged, KNOX-dependent cell fate indeterminacy, (ii) localized organ sculpting and/or (iii) redeployment of hormone-signalling modules. Using cell division markers to guide transcriptome analysis of microdissected spur tissue, we present candidate mechanisms underlying spur outgrowth. We see dynamic expression of factors controlling cell proliferation and hormone signalling, but no evidence of contribution from indeterminacy factors. Transcriptome dynamics point to a novel recruitment event in which auxin-related factors that normally function at the organ margin were co-opted to this central structure. Functional perturbation of the transition between cell division and expansion reveals an unexpected asymmetric component of spur development. These findings indicate that the production of this three-dimensional form is an example of organ sculpting via localized cell division with novel contributions from hormone signalling, rather than a product of prolonged indeterminacy.

}, isbn = {1471-2954 (Electronic)0962-8452 (Linking)}, author = {Yant, L and Collani, S. and Puzey, J. and Levy, C. and Kramer, E. M.} } @article {591866, title = {Floral structure and development in Rafflesiaceae with emphasis on their exceptional gynoecia}, journal = {Am J Bot}, volume = {101}, number = {2}, year = {2014}, note = {

Nikolov, Lachezar AStaedler, Yannick MManickam, SugumaranSchonenberger, JurgEndress, Peter KKramer, Elena MDavis, Charles CengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2014/02/11 06:00Am J Bot. 2014 Feb;101(2):225-43. doi: 10.3732/ajb.1400009. Epub 2014 Feb 8.

}, month = {Feb}, pages = {225-43}, abstract = {

PREMISE OF THE STUDY: The holoparasitic plant family Rafflesiaceae include the world{\textquoteright}s largest flowers. Despite their iconic status, relatively little is known about the morphology and development of their flowers. A recent study clarified the organization of the outer (sterile) floral organs, surprisingly revealing that their distinctive floral chambers arose via different developmental pathways in the two major genera of the family. Here, we expand that research to investigate the structure and development of the reproductive organs of Rafflesiaceae. METHODS: Serial sectioning, scanning electron microscopy, and x-ray tomography of floral buds were employed to reconstruct the structure and development of all three Rafflesiaceae genera. KEY RESULTS: Unlike most angiosperms, which form their shoot apex from the primary morphological surface, the shoot apex of Rafflesiaceae instead forms secondarily via internal cell separation (schizogeny) along the distal boundary of the host-parasite interface. Similarly, the radially directed ovarial clefts of the gynoecium forms via schizogeny within solid tissue, and no carpels are initiated from the floral apex. CONCLUSIONS: The development of the shoot apex and gynoecium of Rafflesiaceae are highly unusual. Although secondary formation of the morphological surface from the shoot apex has been documented in other plant groups, secondary derivation of the inner gynoecium surface is otherwise unknown. Both features are likely synapomorphies of Rafflesiaceae. The secondary derivation of the shoot apex may protect the developing floral shoot as it emerges from within dense host tissue. The secondary formation of the ovarial clefts may generate the extensive placental area necessary to produce hundreds of thousands of ovules.

}, keywords = {Angiosperms/anatomy \& histology/*growth \& development, Flowers/anatomy \& histology/*growth \& development, Meristem/*growth \& development, Ovule/growth \& development}, isbn = {1537-2197 (Electronic)0002-9122 (Linking)}, author = {Nikolov, L. A. and Staedler, Y. M. and Manickam, S. and Schonenberger, J. and Endress, P. K. and Kramer, E. M. and Davis, C.C.} } @article {591861, title = {Holoparasitic Rafflesiaceae possess the most reduced endophytes and yet give rise to the world{\textquoteright}s largest flowers}, journal = {Ann Bot}, volume = {114}, number = {2}, year = {2014}, note = {

Nikolov, Lachezar ATomlinson, P BManickam, SugumaranEndress, Peter KKramer, Elena MDavis, Charles CengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2014/06/20 06:00Ann Bot. 2014 Aug;114(2):233-42. doi: 10.1093/aob/mcu114. Epub 2014 Jun 18.

}, month = {Aug}, pages = {233-42}, abstract = {

BACKGROUND AND AIMS: Species in the holoparasitic plant family Rafflesiaceae exhibit one of the most highly modified vegetative bodies in flowering plants. Apart from the flower shoot and associated bracts, the parasite is a mycelium-like endophyte living inside their grapevine hosts. This study provides a comprehensive treatment of the endophytic vegetative body for all three genera of Rafflesiaceae (Rafflesia, Rhizanthes and Sapria), and reports on the cytology and development of the endophyte, including its structural connection to the host, shedding light on the poorly understood nature of this symbiosis. METHODS: Serial sectioning and staining with non-specific dyes, periodic-Schiff{\textquoteright}s reagent and aniline blue were employed in order to characterize the structure of the endophyte across a phylogenetically diverse sampling. KEY RESULTS: A previously identified difference in the nuclear size between Rafflesiaceae endophytes and their hosts was used to investigate the morphology and development of the endophytic body. The endophytes generally comprise uniseriate filaments oriented radially within the host root. The emergence of the parasite from the host during floral development is arrested in some cases by an apparent host response, but otherwise vegetative growth does not appear to elicit suppression by the host. CONCLUSIONS: Rafflesiaceae produce greatly reduced and modified vegetative bodies even when compared with the other holoparasitic angiosperms once grouped with Rafflesiaceae, which possess some vegetative differentiation. Based on previous studies of seeds together with these findings, it is concluded that the endophyte probably develops directly from a proembryo, and not from an embryo proper. Similarly, the flowering shoot arises directly from the undifferentiated endophyte. These filaments produce a protocorm in which a shoot apex originates endogenously by formation of a secondary morphological surface. This degree of modification to the vegetative body is exceptional within angiosperms and warrants additional investigation. Furthermore, the study highlights a mechanical isolation mechanism by which the host may defend itself from the parasite.

}, keywords = {Angiosperms/*anatomy \& histology/*microbiology, Endophytes/cytology/*physiology, Flowers/*anatomy \& histology, Plant Roots/anatomy \& histology/microbiology, Plant Shoots/microbiology}, isbn = {1095-8290 (Electronic)0305-7364 (Linking)}, author = {Nikolov, L. A. and Tomlinson, P. B. and Manickam, S. and Endress, P. K. and Kramer, E. M. and Davis, C.C.} } @article {591846, title = {STENOFOLIA recruits TOPLESS to repress ASYMMETRIC LEAVES2 at the leaf margin and promote leaf blade outgrowth in Medicago truncatula}, journal = {Plant Cell}, volume = {26}, number = {2}, year = {2014}, note = {

Zhang, FeiWang, YeweiLi, GuifenTang, YuhongKramer, Elena MTadege, MillionengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2014/03/04 06:00Plant Cell. 2014 Feb;26(2):650-64. doi: 10.1105/tpc.113.121947. Epub 2014 Feb 28.

}, month = {Feb}, pages = {650-64}, abstract = {

The Medicago truncatula WUSCHEL-related homeobox (WOX) gene, STENOFOLIA (STF), plays a key role in leaf blade outgrowth by promoting cell proliferation at the adaxial-abaxial junction. STF functions primarily as a transcriptional repressor, but the underlying molecular mechanism is unknown. Here, we report the identification of a protein interaction partner and a direct target, shedding light on the mechanism of STF function. Two highly conserved motifs in the C-terminal domain of STF, the WUSCHEL (WUS) box and the STF box, cooperatively recruit TOPLESS (Mt-TPL) family corepressors, and this recruitment is required for STF function, as deletion of these two domains (STFdel) impaired blade outgrowth whereas fusing Mt-TPL to STFdel restored function. The homeodomain motif is required for direct repression of ASYMMETRIC LEAVES2 (Mt-AS2), silencing of which partially rescues the stf mutant phenotype. STF and LAMINALESS1 (LAM1) are functional orthologs. A single amino acid (Asn to Ile) substitution in the homeodomain abolished the repression of Mt-AS2 and STF{\textquoteright}s ability to complement the lam1 mutant of Nicotiana sylvestris. Our data together support a model in which STF recruits corepressors to transcriptionally repress its targets during leaf blade morphogenesis. We propose that recruitment of TPL/TPL-related proteins may be a common mechanism in the repressive function of modern/WUS clade WOX genes.

}, keywords = {Amino Acid Sequence, Conserved Sequence, Gene Silencing, Medicago truncatula/*growth \& development/*metabolism, Molecular Sequence Data, Phenotype, Plant Leaves/*anatomy \& histology/*growth \& development, Plant Proteins/chemistry/*metabolism, Promoter Regions, Genetic/genetics, Protein Binding, Protein Structure, Tertiary, Repressor Proteins/*metabolism, Structure-Activity Relationship, Tobacco/metabolism}, isbn = {1532-298X (Electronic)1040-4651 (Linking)}, author = {Fei, Z. and Wang, Y. and R. Allen and Kramer, E. M. and Tadege, M.} } @article {591851, title = {Understanding the development and evolution of novel floral form in Aquilegia}, journal = {Curr Opin Plant Biol}, volume = {17}, year = {2014}, note = {

Sharma, BhartiYant, LeviHodges, Scott AKramer, Elena Meng1 F32 GM096699/GM/NIGMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ReviewEngland2014/02/11 06:00Curr Opin Plant Biol. 2014 Feb;17:22-7. doi: 10.1016/j.pbi.2013.10.006. Epub 2013 Nov 15.

}, month = {Feb}, pages = {22-7}, abstract = {

Flowers of the lower eudicot Aquilegia (columbine) possess morphological innovations, namely elaborate petal spurs and a fifth distinct organ identity, the staminodium, that are well suited to the investigation of key questions in developmental evolution. The recent evolution of these characteristics combined with a growing set of genetic and genomic resources has provided insight into how the traits arose and diversified. The petal spur appears to represent a key innovation that diversified largely via modification of specific aspects of cell expansion. In the case of the staminodium, gene duplication has played a role in allowing a novel organ identity to be carved out of the traditional ABC program.

}, keywords = {*Evolution, Molecular, Aquilegia/classification/*genetics/growth \& development, Flowers/*genetics/growth \& development, Gene Duplication, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genetic Variation, Phylogeny, Pigmentation/*genetics, Plant Proteins/genetics}, isbn = {1879-0356 (Electronic)1369-5266 (Linking)}, author = {Sharma, B. and Yant, L and Hodges, S. A. and Kramer, E. M.} } @article {591891, title = {The Aquilegia FRUITFULL-like genes play key roles in leaf morphogenesis and inflorescence development}, journal = {Plant J}, volume = {74}, number = {2}, year = {2013}, note = {

Pabon-Mora, NataliaSharma, BhartiHolappa, Lynn DKramer, Elena MLitt, AmyengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2013/01/09 06:00Plant J. 2013 Apr;74(2):197-212. doi: 10.1111/tpj.12113. Epub 2013 Mar 7.

}, month = {Apr}, pages = {197-212}, abstract = {

The APETALA1/FRUITFULL (AP1/FUL) MADS box transcription factors are best known for the role of AP1 in Arabidopsis sepal and petal identity, the canonical A function of the ABC model of flower development. However, this gene lineage underwent multiple duplication events during angiosperm evolution, providing different taxa with unique gene complements. One such duplication correlates with the origin of the core eudicots, and produced the euAP1 and euFUL clades. Together, euAP1 and euFUL genes function in proper floral meristem identity and repression of axillary meristem growth. Independently, euAP1 genes function in floral meristem and sepal identity, whereas euFUL genes control phase transition, cauline leaf growth and fruit development. To investigate the impact of the core eudicot duplication on the functional diversification of this gene lineage, we studied the role of pre-duplication FUL-like genes in columbine (Aquilegia coerulea). Our results show that AqcFL1 genes are broadly expressed in vegetative and reproductive meristems, leaves and flowers. Virus-induced gene silencing of the loci results in plants with increased branching, shorter inflorescences with fewer flowers, and dramatic changes in leaf shape and complexity. However, aqcfl1 plants have normal flowers and fruits. Our results show that, in contrast to characterized AP1/FUL genes, the AqcFL1 loci are either genetically redundant or have been decoupled from the floral genetic program, and play a major role in leaf morphogenesis. We analyze the results in the context of the core eudicot duplication, and discuss the implications of our findings in terms of the genetic regulation of leaf morphogenesis in Aquilegia and other flowering plants.

}, keywords = {Aquilegia/genetics/*metabolism/*physiology, Flowers/genetics/*metabolism/*physiology, Gene Duplication/genetics/physiology, Gene Expression Regulation, Plant, Plant Leaves/genetics/*metabolism/*physiology, Plant Proteins/genetics/*metabolism}, isbn = {1365-313X (Electronic)0960-7412 (Linking)}, author = {Pabon-Mora, N. and Sharma, B. and Holappa, L. D. and Kramer, E. M. and Litt, A.} } @article {591906, title = {Conserved roles for Polycomb Repressive Complex 2 in the regulation of lateral organ development in Aquilegia x coerulea {\textquoteright}Origami{\textquoteright}}, journal = {BMC Plant Biol}, volume = {13}, year = {2013}, note = {

Gleason, Emily JKramer, Elena MengEngland2013/11/22 06:00BMC Plant Biol. 2013 Nov 20;13:185. doi: 10.1186/1471-2229-13-185.

}, pages = {185}, abstract = {

BACKGROUND: Epigenetic regulation is necessary for maintaining gene expression patterns in multicellular organisms. The Polycomb Group (PcG) proteins form several complexes with important and deeply conserved epigenetic functions in both the plant and animal kingdoms. One such complex, the Polycomb Repressive Complex 2 (PRC2), is critical to many developmental processes in plants including the regulation of major developmental transitions. In addition, PRC2 restricts the expression domain of various transcription factor families in Arabidopsis, including the class I KNOX genes and several of the ABCE class MADS box genes. While the functions of these transcription factors are known to be deeply conserved, whether or not their regulation by PRC2 is similarly conserved remains an open question. RESULTS: Here we use virus-induced gene silencing (VIGS) to characterize the function of the PRC2 complex in lateral organ development of Aquilegia x coerulea {\textquoteright}Origami{\textquoteright}, a member of the lower eudicot order Ranunculales. Leaves with PRC2 down-regulation displayed a range of phenotypes including ruffled or curled laminae, additional lobing, and an increased frequency of higher order branching. Sepals and petals were also affected, being narrowed, distorted, or, in the case of the sepals, exhibiting partial homeotic transformation. Many of the petal limbs also had a particularly intense yellow coloration due to an accumulation of carotenoid pigments. We show that the A. x coerulea floral MADS box genes AGAMOUS1 (AqAG1), APETALA3-3 (AqAP3-3) and SEPALLATA3 (AqSEP3) are up-regulated in many tissues, while expression of the class I KNOX genes and several candidate genes involved in carotenoid production or degradation are largely unaffected. CONCLUSIONS: PRC2 targeting of several floral MADS box genes may be conserved in dicots, but other known targets do not appear to be. In the case of the type I KNOX genes, this may reflect a regulatory shift associated with the evolution of compound leaves.

}, keywords = {*Conserved Sequence, *Crosses, Genetic, *Organogenesis/genetics, Aquilegia/genetics/*growth \& development/*metabolism, Down-Regulation/genetics, Flowers/anatomy \& histology/genetics, Gene Expression Regulation, Plant, Gene Silencing, Genetic Association Studies, Phenotype, Plant Leaves/genetics, Plant Proteins/metabolism, Plant Viruses/physiology, Polycomb Repressive Complex 2/genetics/*metabolism}, isbn = {1471-2229 (Electronic)1471-2229 (Linking)}, author = {Gleason, E. J. and Kramer, E. M.} } @article {591881, title = {The corona of the daffodil Narcissus bulbocodium shares stamen-like identity and is distinct from the orthodox floral whorls}, journal = {Plant J}, volume = {74}, number = {4}, year = {2013}, note = {

Waters, Mark TTiley, Anna M MKramer, Elena MMeerow, Alan WLangdale, Jane AScotland, Robert WengResearch Support, Non-U.S. Gov{\textquoteright}tEngland2013/02/15 06:00Plant J. 2013 May;74(4):615-25. doi: 10.1111/tpj.12150. Epub 2013 Mar 13.

}, month = {May}, pages = {615-25}, abstract = {

The structural homology of the daffodil corona has remained a source of debate throughout the history of botany. Over the years it has been separately referred to as a modified petal stipule, stamen and tepal. Here we provide insights from anatomy and molecular studies to clarify the early developmental stages and position of corona initiation in Narcissus bulbocodium. We demonstrate that the corona initiates as six separate anlagen from hypanthial tissue between the stamens and perianth. Scanning electron microscope images and serial sections demonstrate that corona initiation occurs late in development, after the other floral whorls are fully developed. To define more precisely the identity of the floral structures, daffodil orthologues of the ABC floral organ identity genes were isolated and expression patterns were examined in perianth, stamens, carpel, hypanthial tube and corona tissue. Coupled with in situ hybridisation experiments, these analyses showed that the expression pattern of the C-class gene NbAGAMOUS in the corona is more similar to that of the stamens than that of the tepals. In combination, our results demonstrate that the corona of the daffodil N. bulbocodium exhibits stamen-like identity, develops independently from the orthodox floral whorls and is best interpreted as a late elaboration of the region between the petals and stamens associated with epigyny and the hypanthium.

}, keywords = {*Gene Expression Regulation, Developmental, Flowers/*anatomy \& histology/*genetics/growth \& development, Gene Expression Regulation, Plant, In Situ Hybridization, Liliaceae/anatomy \& histology/genetics/metabolism, MADS Domain Proteins, Microscopy, Electron, Scanning, Models, Biological, Molecular Sequence Data, Narcissus/*anatomy \& histology/*genetics/growth \& development, Phylogeny, Plant Proteins/*genetics/metabolism, RNA, Messenger/genetics, RNA, Plant/genetics}, isbn = {1365-313X (Electronic)0960-7412 (Linking)}, author = {Waters, M. T. and Tiley, A. M. and Kramer, E. M. and Meerow, A. W. and Langdale, J. A. and Scotland, R. W.} } @article {591896, title = {Developmental origins of the world{\textquoteright}s largest flowers, Rafflesiaceae}, journal = {Proc Natl Acad Sci USA}, volume = {110}, number = {46}, year = {2013}, note = {

Nikolov, Lachezar AEndress, Peter KSugumaran, MSasirat, SawitreeVessabutr, SuyaneeKramer, Elena MDavis, Charles CengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2013/10/30 06:00Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18578-83. doi: 10.1073/pnas.1310356110. Epub 2013 Oct 28.

}, month = {Nov 12}, pages = {18578-83}, abstract = {

Rafflesiaceae, which produce the world{\textquoteright}s largest flowers, have captivated the attention of biologists for nearly two centuries. Despite their fame, however, the developmental nature of the floral organs in these giants has remained a mystery. Most members of the family have a large floral chamber defined by a diaphragm. The diaphragm encloses the reproductive organs where pollination by carrion flies occurs. In lieu of a functional genetic system to investigate floral development in these highly specialized holoparasites, we used comparative studies of structure, development, and gene-expression patterns to investigate the homology of their floral organs. Our results surprisingly demonstrate that the otherwise similar floral chambers in two Rafflesiaceae subclades, Rafflesia and Sapria, are constructed very differently. In Rafflesia, the diaphragm is derived from the petal whorl. In contrast, in Sapria it is derived from elaboration of a unique ring structure located between the perianth and the stamen whorl, which, although developed to varying degrees among the genera, appears to be a synapomorphy of the Rafflesiaceae. Thus, the characteristic features that define the floral chamber in these closely related genera are not homologous. These differences refute the prevailing hypothesis that similarities between Sapria and Rafflesia are ancestral in the family. Instead, our data indicate that Rafflesia-like and Sapria-like floral chambers represent two distinct derivations of this morphology. The developmental repatterning we identified in Rafflesia, in particular, may have provided architectural reinforcement, which permitted the explosive growth in floral diameter that has arisen secondarily within this subclade.

}, keywords = {Angiosperms/*growth \& development/metabolism, Base Sequence, Cloning, Molecular, DNA Primers/genetics, DNA, Complementary/biosynthesis, Flowers/*anatomy \& histology/*growth \& development/metabolism, Gene Expression Profiling, Gene Expression Regulation, Developmental/*physiology, Malaysia, Molecular Sequence Data, Reverse Transcriptase Polymerase Chain Reaction, Sequence Analysis, DNA}, isbn = {1091-6490 (Electronic)0027-8424 (Linking)}, author = {Nikolov, L. A. and Endress, P. K. and Sugumaran, M. and Sasirat, S. and Vessabutr, S. and Kramer, E. M. and Davis, C.C.} } @article {591876, title = {Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae)}, journal = {Proc Natl Acad Sci USA}, volume = {110}, number = {13}, year = {2013}, note = {

Zhang, RuiGuo, ChunceZhang, WengenWang, PeipeiLi, LinDuan, XiaoshanDu, QinggaoZhao, LiangShan, HongyanHodges, Scott AKramer, Elena MRen, YiKong, HongzhiengResearch Support, Non-U.S. Gov{\textquoteright}t2013/03/13 06:00Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):5074-9. doi: 10.1073/pnas.1219690110. Epub 2013 Mar 11.

}, month = {Mar 26}, pages = {5074-9}, abstract = {

Absence of petals, or being apetalous, is usually one of the most important features that characterizes a group of flowering plants at high taxonomic ranks (i.e., family and above). The apetalous condition, however, appears to be the result of parallel or convergent evolution with unknown genetic causes. Here we show that within the buttercup family (Ranunculaceae), apetalous genera in at least seven different lineages were all derived from petalous ancestors, indicative of parallel petal losses. We also show that independent petal losses within this family were strongly associated with decreased or eliminated expression of a single floral organ identity gene, APETALA3-3 (AP3-3), apparently owing to species-specific molecular lesions. In an apetalous mutant of Nigella, insertion of a transposable element into the second intron has led to silencing of the gene and transformation of petals into sepals. In several naturally occurring apetalous genera, such as Thalictrum, Beesia, and Enemion, the gene has either been lost altogether or disrupted by deletions in coding or regulatory regions. In Clematis, a large genus in which petalous species evolved secondarily from apetalous ones, the gene exhibits hallmarks of a pseudogene. These results suggest that, as a petal identity gene, AP3-3 has been silenced or down-regulated by different mechanisms in different evolutionary lineages. This also suggests that petal identity did not evolve many times independently across the Ranunculaceae but was lost in numerous instances. The genetic mechanisms underlying the independent petal losses, however, may be complex, with disruption of AP3-3 being either cause or effect.

}, keywords = {*Evolution, Molecular, DNA Transposable Elements/physiology, Flowers/genetics/*metabolism, Gene Expression Regulation, Plant/*physiology, Gene Silencing/physiology, MADS Domain Proteins/*biosynthesis/genetics, Mutagenesis, Insertional, Plant Proteins/*biosynthesis/genetics, Ranunculaceae/genetics/*metabolism}, isbn = {1091-6490 (Electronic)0027-8424 (Linking)}, author = {Zhang, R. and Guo, C. and Zhang, W. and Wang, P. and Li, L. and Duan, X. and Du, Q. and Zhao, L. and Shan, H. and Hodges, S. A. and Kramer, E. M. and Ren, Y. and Kong, H.} } @article {591871, title = {Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors}, journal = {Front Plant Sci}, volume = {4}, year = {2013}, note = {

Zhang, WenhengSteinmann, Victor WNikolov, LachezarKramer, Elena MDavis, Charles CengSwitzerland2013/08/24 06:00Front Plant Sci. 2013 Aug 20;4:302. doi: 10.3389/fpls.2013.00302. eCollection 2013.

}, pages = {302}, abstract = {

Malpighiaceae possess flowers with a unique bilateral symmetry (zygomorphy), which is a hypothesized adaptation associated with specialization on neotropical oil bee pollinators. Gene expression of two representatives of the CYC2 lineage of floral symmetry TCP genes, CYC2A and CYC2B, demarcate the adaxial (dorsal) region of the flower in the characteristic zygomorphic flowers of most Malpighiaceae. Several clades within the family, however, have independently lost their specialized oil bee pollinators and reverted to radial flowers (actinomorphy) like their ancestors. Here, we investigate CYC2 expression associated with four independent reversals to actinomorphy. We demonstrate that these reversals are always associated with alteration of the highly conserved CYC2 expression pattern observed in most New World (NW) Malpighiaceae. In NW Lasiocarpus and Old World (OW) Microsteria, the expression of CYC2-like genes has expanded to include the ventral region of the corolla. Thus, the pattern of gene expression in these species has become radialized, which is comparable to what has been reported in the radial flowered legume clade Cadia. In striking contrast, in NW Psychopterys and OW Sphedamnocarpus, CYC2-like expression is entirely absent or at barely detectable levels. This is more similar to the pattern of CYC2 expression observed in radial flowered Arabidopsis. These results collectively indicate that, regardless of geographic distribution, reversals to similar floral phenotypes in this large tropical angiosperm clade have evolved via different genetic changes from an otherwise highly conserved developmental program.

}, isbn = {1664-462X (Electronic)1664-462X (Linking)}, author = {Zhang, W. and Steinmann, V. W. and Nikolov, L. and Kramer, E. M. and Davis, C.C.} } @article {591911, title = {Pleiotropy in the wild: the dormancy gene DOG1 exerts cascading control on life cycles}, journal = {Evolution}, volume = {67}, number = {3}, year = {2013}, note = {

Chiang, George C KBarua, DeepakDittmar, EmilyKramer, Elena Mde Casas, Rafael RubioDonohue, KathleenengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2013/03/07 06:00Evolution. 2013 Mar;67(3):883-93. doi: 10.1111/j.1558-5646.2012.01828.x. Epub 2012 Nov 16.

}, month = {Mar}, pages = {883-93}, abstract = {

In the wild, organismal life cycles occur within seasonal cycles, so shifts in the timing of developmental transitions can alter the seasonal environment experienced subsequently. Effects of genes that control the timing of prior developmental events can therefore be magnified in the wild because they determine seasonal conditions experienced by subsequent life stages, which can influence subsequent phenotypic expression. We examined such environmentally induced pleiotropy of developmental-timing genes in a field experiment with Arabidopsis thaliana. When studied in the field under natural seasonal variation, an A. thaliana seed-dormancy gene, Delay Of Germination 1 (DOG1), was found to influence not only germination, but also flowering time, overall life history, and fitness. Flowering time of the previous generation, in turn, imposed maternal effects that altered germination, the effects of DOG1 alleles, and the direction of natural selection on these alleles. Thus under natural conditions, germination genes act as flowering genes and potentially vice versa. These results illustrate how seasonal environmental variation can alter pleiotropic effects of developmental-timing genes, such that effects of genes that regulate prior life stages ramify to influence subsequent life stages. In this case, one gene acting at the seed stage impacted the entire life cycle.

}, keywords = {*Plant Dormancy, Arabidopsis Proteins/*genetics, Arabidopsis/*genetics/growth \& development, Flowers/*physiology, Genotype, Selection, Genetic}, isbn = {1558-5646 (Electronic)0014-3820 (Linking)}, author = {Chiang, G. C. and Barua, D. and Dittmar, E. and Kramer, E. M. and de Casas, R. R. and Donohue, K.} } @article {591886, title = {Virus-induced gene silencing in the rapid cycling columbine Aquilegia coerulea "Origami"}, journal = {Methods Mol Biol}, volume = {975}, year = {2013}, note = {

Sharma, BhartiKramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Clifton, N.J.2013/02/07 06:00Methods Mol Biol. 2013;975:71-81. doi: 10.1007/978-1-62703-278-0_6.

}, pages = {71-81}, abstract = {

Aquilegia Origami is an emerging model system for ecology and evolution, which has numerous genetic and genomic tools. Virus-induced gene silencing (VIGS) has been established as an effective approach to study gene function in Aquilegia. In the current protocol, we demonstrate VIGS using Agrobacterium strain GV3101 carrying tobacco rattle virus (TRV)-based constructs to infect Aquilegia coerulea "Origami" plants via vacuum infiltration.

}, keywords = {Agrobacterium tumefaciens/virology, Aquilegia/*genetics/virology, Gene Expression Regulation, Plant, Gene Knockdown Techniques, Genes, Plant, Genetic Vectors, Phenotype, Plant Viruses/*genetics, RNA Interference, Transformation, Bacterial}, isbn = {1940-6029 (Electronic)1064-3745 (Linking)}, author = {Sharma, B. and Kramer, E. M.} } @article {591921, title = {Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets}, journal = {PLoS OnePLoS OnePLoS One}, volume = {7}, number = {3}, year = {2012}, note = {Puzey, Joshua RKarger, AmirAxtell, MichaelKramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2012/03/24 06:00PLoS One. 2012;7(3):e33034. doi: 10.1371/journal.pone.0033034. Epub 2012 Mar 19.}, pages = {e33034}, abstract = {Populus trichocarpa is an important woody model organism whose entire genome has been sequenced. This resource has facilitated the annotation of microRNAs (miRNAs), which are short non-coding RNAs with critical regulatory functions. However, despite their developmental importance, P. trichocarpa miRNAs have yet to be annotated from numerous important tissues. Here we significantly expand the breadth of tissue sampling and sequencing depth for miRNA annotation in P. trichocarpa using high-throughput smallRNA (sRNA) sequencing. miRNA annotation was performed using three individual next-generation sRNA sequencing runs from separate leaves, xylem, and mechanically treated xylem, as well as a fourth run using a pooled sample containing vegetative apices, male flowers, female flowers, female apical buds, and male apical and lateral buds. A total of 276 miRNAs were identified from these datasets, including 155 previously unannotated miRNAs, most of which are P. trichocarpa specific. Importantly, we identified several xylem-enriched miRNAs predicted to target genes known to be important in secondary growth, including the critical reaction wood enzyme xyloglucan endo-transglycosylase/hydrolase and vascular-related transcription factors. This study provides a thorough genome-wide annotation of miRNAs in P. trichocarpa through deep sRNA sequencing from diverse tissue sets. Our data significantly expands the P. trichocarpa miRNA repertoire, which will facilitate a broad range of research in this major model system.}, keywords = {*Databases, Genetic, *Molecular Sequence Annotation, MicroRNAs/*genetics, Ovule/genetics, Pollen/genetics, Populus/*genetics, RNA, Plant/*genetics}, isbn = {1932-6203 (Electronic)1932-6203 (Linking)}, author = {Puzey, J. R. and Karger, A. and Axtell, M. and Kramer, E. M.} } @article {591916, title = {Similar genetic mechanisms underlie the parallel evolution of floral phenotypes}, journal = {PLoS OnePLoS OnePLoS One}, volume = {7}, number = {4}, year = {2012}, note = {Zhang, WenhengKramer, Elena MDavis, Charles CengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2012/05/05 06:00PLoS One. 2012;7(4):e36033. doi: 10.1371/journal.pone.0036033. Epub 2012 Apr 27.}, pages = {e36033}, abstract = {The repeated origin of similar phenotypes is invaluable for studying the underlying genetics of adaptive traits; molecular evidence, however, is lacking for most examples of such similarity. The floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to result from specialization on oil-bee pollinators. We recently demonstrated that CYCLOIDEA2-like genes (CYC2A and CYC2B) are associated with the development of the stereotypical floral zygomorphy that is critical to this plant-pollinator mutualism. Here, we build on this developmental framework to characterize floral symmetry in three clades of Malpighiaceae that have independently lost their oil bee association and experienced parallel shifts in their floral morphology, especially in regard to symmetry. We show that in each case these species exhibit a loss of CYC2B function, and a strikingly similar shift in the expression of CYC2A that is coincident with their shift in floral symmetry. These results indicate that similar floral phenotypes in this large angiosperm clade have evolved via parallel genetic changes from an otherwise highly conserved developmental program.}, keywords = {*Biological Evolution, Flowers/*anatomy \& histology/*genetics/growth \& development/ultrastructure, Gene Expression Regulation, Plant, Genes, Plant/genetics, Malpighiaceae/*anatomy \& histology/*genetics/ultrastructure, Phenotype, Phylogeny, Plant Proteins/genetics/metabolism, Reverse Transcriptase Polymerase Chain Reaction}, isbn = {1932-6203 (Electronic)1932-6203 (Linking)}, author = {Zhang, W. and Kramer, E. M. and Davis, C.C.} } @article {591936, title = {Characterization of Aquilegia Polycomb Repressive Complex 2 homologs reveals absence of imprinting}, journal = {Gene}, volume = {507}, number = {1}, year = {2012}, note = {

Gleason, Emily JKramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Netherlands2012/07/17 06:00Gene. 2012 Oct 1;507(1):54-60. doi: 10.1016/j.gene.2012.07.004. Epub 2012 Jul 13.

}, month = {Oct 1}, pages = {54-60}, abstract = {

Epigenetic regulation is important for maintaining gene expression patterns in multicellular organisms. The Polycomb Group (PcG) proteins form several complexes with important and deeply conserved epigenetic functions in both the plant and animal kingdoms. The plant Polycomb Repressive Complex 2 (PRC2) contains four core proteins, Enhancer of Zeste (E(z)), Suppressor of Zeste 12 (Su(z)12), Extra Sex Combs (ESC), and Multicopy Suppressor of IRA 1 (MSI1), and functions in many developmental transitions. In some plant species, including rice and Arabidopsis, duplications in the core PRC2 proteins allow the formation of PRC2s with distinct developmental functions. In addition, members of the plant specific VEL PHD family have been shown to associate with the PRC2 complex in Arabidopsis and may play a role in targeting the PRC2 to specific loci. Here we examine the evolution and expression of the PRC2 and VEL PHD families in Aquilegia, a member of the lower eudicot order Ranunculales and an emerging model for the investigation of plant ecology, evolution and developmental genetics. We find that Aquilegia has a relatively simple PRC2 with only one homolog of Su(z)12, ESC and MSI1 and two ancient copies of E(z), AqSWN and AqCLF. Aquilegia has four members of the VEL PHD family, three of which appear to be closely related to Arabidopsis proteins known to associate with the PRC2. The PRC2 and VEL PHD family proteins are expressed at a relatively constant level throughout Aquilegia vulgaris development, with the VEL PHD family and MSI1 expressed at higher levels during and after vernalization and in the inflorescence. Both AqSWN and AqCLF are expressed in Aquilegia endosperm but neither copy is imprinted.

}, keywords = {*Genomic Imprinting, Aquilegia/*genetics, Arabidopsis/genetics/metabolism, Evolution, Molecular, Gene Expression Regulation, Plant, Genome, Plant, Phylogeny, Plant Proteins/*genetics/metabolism, Polycomb-Group Proteins, Repressor Proteins/*genetics}, isbn = {1879-0038 (Electronic)0378-1119 (Linking)}, author = {Gleason, E. J. and Kramer, E. M.} } @article {591931, title = {The evolution of reproductive structures in seed plants: a re-examination based on insights from developmental genetics}, journal = {New Phytol}, volume = {194}, number = {4}, year = {2012}, note = {

Mathews, SarahKramer, Elena MengReviewEngland2012/03/15 06:00New Phytol. 2012 Jun;194(4):910-23. doi: 10.1111/j.1469-8137.2012.04091.x. Epub 2012 Mar 13.

}, month = {Jun}, pages = {910-23}, abstract = {

The study of developmental genetics is providing insights into how plant morphology can and does evolve, and into the fundamental nature of specific organs. This new understanding has the potential to revise significantly the way we think about seed plant evolution, especially with regard to reproductive structures. Here, we have sought to take a step in bridging the divide between genetic data and critical fields such as paleobotany and systematics. We discuss the evidence for several evolutionarily important interpretations, including the possibility that ovules represent meristematic axes with their own type of lateral determinate organs (integuments) and a model that considers carpels as analogs of complex leaves. In addition, we highlight the aspects of reproductive development that are likely to be highly labile and homoplastic, factors that have major implications for the understanding of seed plant relationships. Although these hypotheses may suggest that some long-standing interpretations are misleading, they also open up whole new avenues for comparative study and suggest concrete best practices for evolutionary analyses of development.

}, keywords = {*Biological Evolution, *Flowers, Arabidopsis/*genetics/growth \& development}, isbn = {1469-8137 (Electronic)0028-646X (Linking)}, author = {Mathews, S. and Kramer, E. M.} } @article {591926, title = {Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy}, journal = {Proc Biol Sci}, volume = {279}, number = {1733}, year = {2012}, note = {

Puzey, Joshua RGerbode, Sharon JHodges, Scott AKramer, Elena MMahadevan, LengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2011/11/18 06:00Proc Biol Sci. 2012 Apr 22;279(1733):1640-5. doi: 10.1098/rspb.2011.1873. Epub 2011 Nov 16.

}, month = {Apr 22}, pages = {1640-5}, abstract = {

The role of petal spurs and specialized pollinator interactions has been studied since Darwin. Aquilegia petal spurs exhibit striking size and shape diversity, correlated with specialized pollinators ranging from bees to hawkmoths in a textbook example of adaptive radiation. Despite the evolutionary significance of spur length, remarkably little is known about Aquilegia spur morphogenesis and its evolution. Using experimental measurements, both at tissue and cellular levels, combined with numerical modelling, we have investigated the relative roles of cell divisions and cell shape in determining the morphology of the Aquilegia petal spur. Contrary to decades-old hypotheses implicating a discrete meristematic zone as the driver of spur growth, we find that Aquilegia petal spurs develop via anisotropic cell expansion. Furthermore, changes in cell anisotropy account for 99 per cent of the spur-length variation in the genus, suggesting that the true evolutionary innovation underlying the rapid radiation of Aquilegia was the mechanism of tuning cell shape.

}, keywords = {*Cell Shape, Anisotropy, Aquilegia/*anatomy \& histology/cytology/growth \& development, Biological Evolution, Flowers/anatomy \& histology/cytology/growth \& development, Meristem/cytology/growth \& development/physiology, Pollination}, isbn = {1471-2954 (Electronic)0962-8452 (Linking)}, author = {Puzey, J. R. and Gerbode, S. J. and Hodges, S. A. and Kramer, E. M. and Mahadevan, L.} } @article {591941, title = {Understanding the basis of a novel fruit type in Brassicaceae: conservation and deviation in expression patterns of six genes}, journal = {Evodevo}, volume = {3}, number = {1}, year = {2012}, note = {

Avino, MarianoKramer, Elena MDonohue, KathleenHammel, Alexander JHall, Jocelyn CengEngland2012/09/05 06:00Evodevo. 2012 Sep 3;3(1):20. doi: 10.1186/2041-9139-3-20.

}, pages = {20}, abstract = {

BACKGROUND: Variation in fruit morphology is important for plant fitness because it influences dispersal capabilities. Approximately half the members of tribe Brassiceae (Brassicaceae) exhibit fruits with segmentation and variable dehiscence, called heteroarthrocarpy. The knowledge of the genetics of fruit patterning in Arabidopsis offers the opportunity to ask: (1) whether this genetic pathway is conserved in taxa with different fruit morphologies; (2) how the pathway may be modified to produce indehiscence; and (3) whether the pathway has been recruited for a novel abscission zone. METHODS: We identified homologs of ALCATRAZ, FRUITFULL, INDEHISCENT, SHATTERPROOF, and REPLUMLESS from two taxa, representing different types of heteroarthrocarpy. Comparative gene expression of twelve loci was assessed to address how their expression may have been modified to produce heteroarthrocarpy. RESULTS: Studies demonstrated overall conservation in gene expression patterns between dehiscent segments of Erucaria erucarioides and Arabidopsis, with some difference in expression of genes that position the valve margin. In contrast, indehiscence in heteroarthrocarpic fruit segments was correlated with the elimination of the entire valve margin pathway in Erucaria and Cakile lanceolata as well as its absence from a novel lateral abscission zone. CONCLUSIONS: These findings suggest that modifications in the valve margin positioning genes are responsible for differences between heteroarthrocarpic and Arabidopsis-like fruits and support the hypothesis that heteroarthrocarpy evolved via repositioning the valve margin. They also highlight conservation in the dehiscence pathway across Brassicaceae.

}, isbn = {2041-9139 (Electronic)2041-9139 (Linking)}, author = {Avino, M. and Kramer, E. M. and Donohue, K. and Hammel, A. J. and Hall, J. C.} } @article {591961, title = {Convergent evolution of a complex fruit structure in the tribe Brassiceae (Brassicaceae)}, journal = {Am J Bot}, volume = {98}, number = {12}, year = {2011}, note = {

Hall, Jocelyn CTisdale, Tracy EDonohue, KathleenWheeler, AndrewAl-Yahya, Mohammed AKramer, Elena MengResearch Support, Non-U.S. Gov{\textquoteright}t2011/11/15 06:00Am J Bot. 2011 Dec;98(12):1989-2003. doi: 10.3732/ajb.1100203. Epub 2011 Nov 11.

}, month = {Dec}, pages = {1989-2003}, abstract = {

PREMISE OF STUDY: Many angiosperms have fruit morphologies that result in seeds from the same plant having different dispersal capabilities. A prime example is found in the Brassiceae (Brassicaceae), which has many members with segmented or heteroarthrocarpic fruits. Since only 40\% of the genera are heteroarthrocarpic, this tribe provides an opportunity to study the evolution of an ecologically significant novelty and its variants. METHODS: We analyzed nuclear (PHYA) and plastid (matK) sequences from 66 accessions using maximum parsimony, maximum likelihood, and Bayesian inference approaches. The evolution of heteroarthrocarpy and its variants was evaluated using maximum parsimony and maximum likelihood ancestral state reconstructions. KEY RESULTS: Although nuclear and plastid phylogenies are incongruent with each other, the following findings are consistent: (1) Cakile, Crambe, Vella, and Zilla lineages are monophyletic; (2) the Nigra lineage is not monophyletic; and (3) within the Cakile clade, Cakile, Didesmus, and Erucaria are paraphyletic. Despite differences in the matK and PHYA topologies at both deep and shallow nodes, similar patterns of morphological evolution emerge. Heteroarthrocarpy, a complex morphological trait, has evolved multiple times across the tribe. Moreover, there are convergent transitions in dehiscence capabilities and fruit disarticulation across the tribe. CONCLUSIONS: We present the first explicit analysis of fruit evolution within the Brassiceae, which exemplifies evolutionary lability. The repeated loss and gain of segment dehiscence and disarticulation suggests conservation in the genetic pathway controlling abscission with differential expression across taxa. This study provides a strong foundation for future studies of mechanisms underlying variation in dispersal capabilities of Brassiceae.

}, keywords = {*Biological Evolution, Base Sequence, Bayes Theorem, Brassicaceae/*anatomy \& histology/*genetics, Endoribonucleases/genetics, Fruit/*anatomy \& histology/*genetics/growth \& development, Genes, Plant/genetics, Likelihood Functions, Nucleotidyltransferases/genetics, Phylogeny, Phytochrome A/genetics, Seed Dispersal/genetics}, isbn = {1537-2197 (Electronic)0002-9122 (Linking)}, author = {Hall, J. C. and Tisdale, T. E. and Donohue, K. and Wheeler, A. and Al-Yahya, M. A. and Kramer, E. M.} } @article {591971, title = {Environmental and molecular analysis of the floral transition in the lower eudicot Aquilegia formosa}, journal = {Evodevo}, volume = {2}, year = {2011}, note = {

Ballerini, Evangeline SKramer, Elena MengEngland2011/02/19 06:00Evodevo. 2011 Feb 17;2:4. doi: 10.1186/2041-9139-2-4.

}, pages = {4}, abstract = {

BACKGROUND: Flowering is a critical transition in plant development, the timing of which can have considerable fitness consequences. Until recently, research into the genetic control of flowering time and its associated developmental changes was focused on core eudicots (for example, Arabidopsis) or monocots (for example, Oryza). Here we examine the flowering response of Aquilegia formosa, a member of the eudicot order Ranunculales that is emerging as an important model for the investigation of plant ecology and evolution. RESULTS: We have determined that A. formosa has a strong vernalization requirement but little or no photoperiod response, making it a day neutral (DN) plant. Consistent with this, the Aquilegia homolog of FLOWERING LOCUS T (AqFT) is expressed in both long and short days but surprisingly, the locus is expressed before the transition to flowering. In situ hybridizations with homologs of several Arabidopsis Floral Pathway Integrators (FPIs) do not suggest conserved functions relative to Arabidopsis, the potential exceptions being AqLFY and AqAGL24.2. CONCLUSIONS: In Aquilegia, vernalization is critical to flowering but this signal is not strictly required for the transcriptional activation of AqFT. The expression patterns of AqLFY and AqAGL24.2 suggest a hypothesis for the development of Aquilegia{\textquoteright}s determinate inflorescence whereby their differential expression controls the progression of each meristem from inflorescence to floral identity. Interestingly, none of the Aquilegia expression patterns are consistent with a function in floral repression which, combined with the lack of a FLC homolog, means that new candidate genes must be identified for the control of vernalization response in Aquilegia.

}, isbn = {2041-9139 (Electronic)2041-9139 (Linking)}, author = {Ballerini, E. S. and Kramer, E. M.} } @article {591966, title = {In the Light of Evolution: A Reevaluation of Conservation in the CO-FT Regulon and Its Role in Photoperiodic Regulation of Flowering Time}, journal = {Front Plant Sci}, volume = {2}, year = {2011}, note = {

Ballerini, Evangeline SKramer, Elena MengSwitzerland2011/01/01 00:00Front Plant Sci. 2011 Nov 16;2:81. doi: 10.3389/fpls.2011.00081. eCollection 2011.

}, pages = {81}, abstract = {

In order to maximize reproductive success, plants have evolved different strategies to control the critical developmental shift marked by the transition to flowering. As plants have adapted to diverse environments across the globe, these strategies have evolved to recognize and respond to local seasonal cues through the induction of specific downstream genetic pathways, thereby ensuring that the floral transition occurs in favorable conditions. Determining the genetic factors involved in controlling the floral transition in many species is key to understanding how this trait has evolved. Striking genetic discoveries in Arabidopsis thaliana (Arabidopsis) and Oryza sativa (rice) revealed that similar genes in both species control flowering in response to photoperiod, suggesting that this genetic module could be conserved between distantly related angiosperms. However, as we have gained a better understanding of the complex evolution of these genes and their functions in other species, another possibility must be considered: that the genetic module controlling flowering in response to photoperiod is the result of convergence rather than conservation. In this review, we show that while data clearly support a central role of FLOWERING LOCUS T (FT) homologs in floral promotion across a diverse group of angiosperms, there is little evidence for a conserved role of CONSTANS (CO) homologs in the regulation of these loci. In addition, although there is an element of conserved function for FT homologs, even this component has surprising complexity in its regulation and evolution.

}, isbn = {1664-462X (Electronic)1664-462X (Linking)}, author = {Ballerini, E. S. and Kramer, E. M.} } @article {591946, title = {Petal-specific subfunctionalization of an APETALA3 paralog in the Ranunculales and its implications for petal evolution}, journal = {New Phytol}, volume = {191}, number = {3}, year = {2011}, note = {

Sharma, BhartiGuo, ChunceKong, HongzhiKramer, Elena MengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2011/05/12 06:00New Phytol. 2011 Aug;191(3):870-83. doi: 10.1111/j.1469-8137.2011.03744.x. Epub 2011 May 9.

}, month = {Aug}, pages = {870-83}, abstract = {

* The petals of the lower eudicot family Ranunculaceae are thought to have been derived many times independently from stamens. However, investigation of the genetic basis of their identity has suggested an alternative hypothesis: that they share a commonly inherited petal identity program. This theory is based on the fact that an ancient paralogous lineage of APETALA3 (AP3) in the Ranunculaceae appears to have a conserved, petal-specific expression pattern. * Here, we have used a combination of approaches, including RNAi, comparative gene expression and molecular evolutionary studies, to understand the function of this petal-specific AP3 lineage. * Functional analysis of the Aquilegia locus AqAP3-3 has demonstrated that the paralog is required for petal identity with little contribution to the identity of the other floral organs. Expanded expression studies and analyses of molecular evolutionary patterns provide further evidence that orthologs of AqAP3-3 are primarily expressed in petals and are under higher purifying selection across the family than the other AP3 paralogs. * Taken together, these findings suggest that the AqAP3-3 lineage underwent progressive subfunctionalization within the order Ranunculales, ultimately yielding a specific role in petal identity that has probably been conserved, in stark contrast with the multiple independent origins predicted by botanical theories.

}, keywords = {*Biological Evolution, Amino Acid Sequence, Aquilegia/anatomy \& histology/genetics/*metabolism, Flowers/*anatomy \& histology/genetics/metabolism, Gene Expression Regulation, Plant/genetics, Genes, Plant/genetics, Molecular Sequence Data, Organ Specificity/genetics, Phenotype, Phylogeny, Plant Proteins/genetics/*metabolism, Ranunculaceae/anatomy \& histology/genetics/*metabolism, RNA Interference, Sequence Homology, Amino Acid}, isbn = {1469-8137 (Electronic)0028-646X (Linking)}, author = {Sharma, B. and Guo, C. and Kong, H. and Kramer, E. M.} } @article {591986, title = {The ABC model and the diversification of floral organ identity}, journal = {Semin Cell Dev Biol}, volume = {21}, number = {1}, year = {2010}, note = {

Litt, AmyKramer, Elena MengReviewEngland2009/12/02 06:00Semin Cell Dev Biol. 2010 Feb;21(1):129-37. doi: 10.1016/j.semcdb.2009.11.019. Epub 2009 Dec 3.

}, month = {Feb}, pages = {129-37}, abstract = {

Broad studies of the ABC program across angiosperms have found that interactions between gene duplication, biochemical evolution, shifts in gene expression and modification of existing identity programs have been critical to the evolution of floral morphology. Several themes can be recognized in this context. First, the original concept of "A" function applies only very narrowly to Arabidopsis and its close relatives. Second, while many types of petaloid organs are associated with the expression of AP3/PI homologs, there is growing evidence that there are other genetic mechanisms for producing petaloidy, especially in first whorl organs. Third, pre-existing organ identity programs can be modified to yield novel organ types, often in association with gene duplications. Lastly, there are many aspects of ABC gene function outside the major model systems that remain a mystery, perhaps none more so than the C-terminal amino acid motifs that distinguish specific ABC gene lineages.

}, keywords = {*Flowers/anatomy \& histology/classification/physiology, *Gene Expression Regulation, Plant, Arabidopsis/anatomy \& histology/physiology, Biological Evolution, Gene Duplication, MADS Domain Proteins/*genetics/metabolism, Models, Biological, Phylogeny, Plant Proteins/*genetics/metabolism}, isbn = {1096-3634 (Electronic)1084-9521 (Linking)}, author = {Litt, A. and Kramer, E. M.} } @article {591991, title = {Aquilegia as a model system for the evolution and ecology of petals}, journal = {Philos Trans R Soc Lond B Biol Sci}, volume = {365}, number = {1539}, year = {2010}, note = {

Kramer, Elena MHodges, Scott AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ReviewEngland2010/01/06 06:00Philos Trans R Soc Lond B Biol Sci. 2010 Feb 12;365(1539):477-90. doi: 10.1098/rstb.2009.0230.

}, month = {Feb 12}, pages = {477-90}, abstract = {

The ranunculid genus Aquilegia holds extraordinary promise as a model system for investigating a wide range of questions relating to the evolution and ecology of petals. New genetic and genomic resources, including an extensive EST database, BAC libraries and physical maps, as well as virus-induced gene silencing are facilitating this research on multiple fronts. At the developmental genetic level, Aquilegia has been important for elucidating the developmental programme for specifying petals and petaloid characteristics. Data suggest that duplication events among the petal and stamen identity genes have resulted in sub- and neofunctionalization. This expansion of gene function does not include the petaloidy of Aquilegia sepals, however, which does not depend on the same loci that control identity of the second whorl petals. Of special interest is the elaboration of the petal into a nectar spur, a major innovation for the genus. Intra- and interspecific variation in the shape and colour of petals, especially the spurs, has been shown to be adaptative for different pollinators. Thus, understanding the genetic basis of these traits will help us connect the ecological interactions driving speciation with the genetic changes responsible for remodelling morphology. Progress in this area has focused on the multiple, parallel transitions in flower colour and nectar spur length across the genus. For flower colour, upstream transcription factors appear to be primarily targets of natural selection. Thus research in Aquilegia spans the initial evolution of petals and petaloidy to the diversification of petal morphology to the ecological basis of petal form, thereby providing a comprehensive picture of the evolutionary biology of this critical angiosperm feature.

}, keywords = {*Evolution, Molecular, *Gene Duplication, Aquilegia/anatomy \& histology/*genetics, Expressed Sequence Tags, Flowers/anatomy \& histology/*genetics, Gene Library, Phylogeny}, isbn = {1471-2970 (Electronic)0962-8436 (Linking)}, author = {Kramer, E. M. and Hodges, S. A.} } @article {591976, title = {Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism}, journal = {Proc Natl Acad Sci USA}, volume = {107}, number = {14}, year = {2010}, note = {

Zhang, WenhengKramer, Elena MDavis, Charles CengResearch Support, Non-U.S. Gov{\textquoteright}t2010/04/07 06:00Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6388-93. doi: 10.1073/pnas.0910155107. Epub 2010 Apr 2.

}, month = {Apr 6}, pages = {6388-93}, abstract = {

The evolution of floral zygomorphy is an important innovation in flowering plants and is thought to arise principally from specialization on various insect pollinators. Floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to be caused by selection by its oil-bee pollinators. We sought to characterize the genetic basis of floral zygomorphy in Malpighiaceae by investigating CYCLOIDEA2-like (CYC2-like) genes, which are required for establishing symmetry in diverse core eudicots. We identified two copies of CYC2-like genes in Malpighiaceae, which resulted from a gene duplication in the common ancestor of the family. A likely role for these loci in the development of floral zygomorphy in Malpighiaceae is demonstrated by the conserved pattern of dorsal gene expression in two distantly related neotropical species, Byrsonima crassifolia and Janusia guaranitica. Further evidence for this function is observed in a Malpighiaceae species that has moved to the paleotropics and experienced coincident shifts in pollinators, floral symmetry, and CYC2-like gene expression. The dorsal expression pat-tern observed in Malpighiaceae contrasts dramatically with their actinomorphic-flowered relatives, Centroplacaceae (Bhesa paniculata) and Elatinaceae (Bergia texana). In particular, B. texana exhibits a previously undescribed pattern of uniform CYC2 expression, suggesting that CYC2 expression among the actinomorphic ancestors of zygomorphic lineages may be much more complex than previously thought. We consider three evolutionary models that may have given rise to this patterning, including the hypothesis that floral zygomorphy in Malpighiaceae arose earlier than standard morphology-based character reconstructions suggest.

}, keywords = {*Pollination, *Symbiosis, DNA-Binding Proteins, Flowers/*anatomy \& histology/*genetics/physiology, Gene Duplication, Gene Expression Regulation, Plant, Molecular Sequence Data, Phylogeny, Plant Proteins/genetics, Transcription Factors}, isbn = {1091-6490 (Electronic)0027-8424 (Linking)}, author = {Zhang, W. and Kramer, E. M. and Davis, C.C.} } @article {591981, title = {Within and between whorls: comparative transcriptional profiling of Aquilegia and Arabidopsis}, journal = {PLoS One}, volume = {5}, number = {3}, year = {2010}, note = {

Voelckel, ClaudiaBorevitz, Justin OKramer, Elena MHodges, Scott AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2010/03/31 06:00PLoS One. 2010 Mar 23;5(3):e9735. doi: 10.1371/journal.pone.0009735.

}, pages = {e9735}, abstract = {

BACKGROUND: The genus Aquilegia is an emerging model system in plant evolutionary biology predominantly because of its wide variation in floral traits and associated floral ecology. The anatomy of the Aquilegia flower is also very distinct. There are two whorls of petaloid organs, the outer whorl of sepals and the second whorl of petals that form nectar spurs, as well as a recently evolved fifth whorl of staminodia inserted between stamens and carpels. METHODOLOGY/PRINCIPAL FINDINGS: We designed an oligonucleotide microarray based on EST sequences from a mixed tissue, normalized cDNA library of an A. formosa x A. pubescens F2 population representing 17,246 unigenes. We then used this array to analyze floral gene expression in late pre-anthesis stage floral organs from a natural A. formosa population. In particular, we tested for gene expression patterns specific to each floral whorl and to combinations of whorls that correspond to traditional and modified ABC model groupings. Similar analyses were performed on gene expression data of Arabidopsis thaliana whorls previously obtained using the Ath1 gene chips (data available through The Arabidopsis Information Resource). CONCLUSIONS/SIGNIFICANCE: Our comparative gene expression analyses suggest that 1) petaloid sepals and petals of A. formosa share gene expression patterns more than either have organ-specific patterns, 2) petals of A. formosa and A. thaliana may be independently derived, 3) staminodia express B and C genes similar to stamens but the staminodium genetic program has also converged on aspects of the carpel program and 4) staminodia have unique up-regulation of regulatory genes and genes that have been implicated with defense against microbial infection and herbivory. Our study also highlights the value of comparative gene expression profiling and the Aquilegia microarray in particular for the study of floral evolution and ecology.

}, keywords = {Aquilegia/*genetics, Arabidopsis/*genetics, Cell Cycle, DNA Primers/genetics, DNA, Complementary/metabolism, Evolution, Molecular, Expressed Sequence Tags, Flowers, Gene Expression Profiling, Gene Expression Regulation, Plant, Nucleic Acid Hybridization, Oligonucleotide Array Sequence Analysis}, isbn = {1932-6203 (Electronic)1932-6203 (Linking)}, author = {Voelckel, C. and Borevitz, J. O. and Kramer, E. M. and Hodges, S. A.} } @article {592021, title = {Aquilegia: a new model for plant development, ecology, and evolution}, journal = {Annu Rev Plant Biol}, volume = {60}, year = {2009}, note = {

Kramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2009/07/07 09:00Annu Rev Plant Biol. 2009;60:261-77. doi: 10.1146/annurev.arplant.043008.092051.

}, pages = {261-77}, abstract = {

The lower eudicot genus Aquilegia holds enormous potential for investigating aspects of development, ecology, and evolution that are otherwise unrepresented among existing model systems. Its evolutionary history is of particular interest because it represents a phylogenetic midpoint between models such as Arabidopsis and Oryza but, at the same time, has experienced a recent adaptive radiation within the genus. To take advantage of these features, a collaborative group has developed a number of genetic and genomic resources for Aquilegia that have facilitated the study of its distinct morphology. This work has demonstrated that although the petaloid sepals of Aquilegia do not depend on B-class genes for their identity, these loci do control development of the petals, stamens, and novel staminodium. Overall, Aquilegia stands as a key example of the potential utility and speed of developing new genetic model systems.

}, keywords = {*Biological Evolution, *Ecology, Aquilegia/genetics/*physiology, Genome, Plant}, isbn = {1545-2123 (Electronic)1543-5008 (Linking)}, author = {Kramer, E. M.} } @article {592011, title = {Chapter 4. New model systems for the study of developmental evolution in plants}, journal = {Curr Top Dev Biol}, volume = {86}, year = {2009}, note = {

Kramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Review2009/04/14 09:00Curr Top Dev Biol. 2009;86:67-105. doi: 10.1016/S0070-2153(09)01004-7.

}, pages = {67-105}, abstract = {

The number of genetically tractable plant model systems is rapidly increasing, thanks to the decreasing cost of sequencing and the wide amenability of plants to stable transformation and other functional approaches. In this chapter, I discuss emerging model systems from throughout the land plant phylogeny and consider how their unique attributes are contributing to our understanding of development, evolution, and ecology. These new models are being developed using two distinct strategies: in some cases, they are selected because of their close relationship to the established models, while in others, they are chosen with the explicit intention of exploring distantly related plant lineages. Such complementary approaches are yielding exciting new results that shed light on both micro- and macroevolutionary processes in the context of developmental evolution.

}, keywords = {*Biological Evolution, *Models, Biological, *Plant Physiological Phenomena, Angiosperms/embryology/physiology, Arabidopsis/embryology/physiology, Brassicaceae/embryology/physiology, Bryopsida/embryology/physiology, Ferns/embryology/physiology, Growth and Development/*physiology, Phylogeny, Selaginellaceae/embryology/physiology}, isbn = {0070-2153 (Print)0070-2153 (Linking)}, author = {Kramer, E. M.} } @article {592006, title = {Identification of conserved Aquilegia coerulea microRNAs and their targets}, journal = {Gene}, volume = {448}, number = {1}, year = {2009}, note = {

Puzey, Joshua RKramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Netherlands2009/08/25 09:00Gene. 2009 Dec 1;448(1):46-56. doi: 10.1016/j.gene.2009.08.005. Epub 2009 Aug 19.

}, month = {Dec 1}, pages = {46-56}, abstract = {

Aquilegia is an emerging model organism that is phylogenetically intermediate between the core eudicot and monocot models, Arabidopsis and Oryza. In this study, we have used a comparative genomics approach to identify 45 Aquilegia microRNAs that comprise 20 separate plant microRNA families. We have predicted 84 targets of these newly identified Aquilegia microRNAs including transcription factors and loci involved in metabolism, stress responses, transport, and auxin signaling. microRNA families from 16 plant species and the newly identified microRNAs from Aquilegia were analyzed in a phylogenetic context revealing 40 distantly conserved microRNA families. In addition to these highly conserved plant microRNA families, several families with disjointed phylogenetic distribution were identified. This study provides a phylogenetically important dataset for plant microRNA evolution studies. The current study is the first to identify miRNAs in a lower eudicot in which comprehensive genomic resources are becoming available.

}, keywords = {*Phylogeny, Aquilegia/*genetics, Base Sequence, Carbohydrate Conformation, Databases, Nucleic Acid, Genome, Plant, MicroRNAs/chemistry/*genetics, Molecular Sequence Data, RNA, Plant/chemistry/*genetics}, isbn = {1879-0038 (Electronic)0378-1119 (Linking)}, author = {Puzey, J. R. and Kramer, E. M.} } @article {592031, title = {Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana}, journal = {Proc Natl Acad Sci USA}, volume = {106}, number = {28}, year = {2009}, note = {

Chiang, George C KBarua, DeepakKramer, Elena MAmasino, Richard MDonohue, KathleenengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2009/07/01 09:00Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11661-6. doi: 10.1073/pnas.0901367106. Epub 2009 Jun 29.

}, month = {Jul 14}, pages = {11661-6}, abstract = {

Flowering locus C (FLC) is a major regulator of flowering responses to seasonal environmental factors. Here, we document that FLC also regulates another major life-history transition-seed germination, and that natural variation at the FLC locus and in FLC expression is associated with natural variation in temperature-dependent germination. FLC-mediated germination acts through additional genes in the flowering pathway (FT, SOC1, and AP1) before involving the abscisic acid catabolic pathway (via CYP707A2) and gibberellins biosynthetic pathway (via GA20ox1) in seeds. Also, FLC regulation of germination is largely maternally controlled, with FLC peaking and FT, SOC1, and AP1 levels declining at late stages of seed maturation. High FLC expression during seed maturation is associated with altered expression of hormonal genes (CYP707A2 and GA20ox1) in germinating seeds, indicating that gene expression before the physiological independence of seeds can influence gene expression well after any physical connection between maternal plants and seeds exists. The major role of FLC in temperature-dependent germination documented here reveals a much broader adaptive significance of natural variation in FLC. Therefore, pleiotropy between these major life stages likely influences patterns of natural selection on this important gene, making FLC a promising case for examining how pleiotropy influences adaptive evolution.

}, keywords = {*Genetic Variation, Adaptation, Biological/genetics, Arabidopsis Proteins/*genetics/metabolism, Arabidopsis/*genetics, Flowers/*genetics, Gene Expression Regulation, Plant/*genetics, Germination/*genetics, MADS Domain Proteins/*genetics/metabolism, Seeds/metabolism, Temperature}, isbn = {1091-6490 (Electronic)0027-8424 (Linking)}, author = {Chiang, G. C. and Barua, D. and Kramer, E. M. and Amasino, R. M. and Donohue, K.} } @article {591996, title = {Old dogs, new tricks: regulatory evolution in conserved genetic modules leads to novel morphologies in plants}, journal = {Dev Biol}, volume = {332}, number = {1}, year = {2009}, note = {

Rosin, Faye MKramer, Elena MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Review2009/05/13 09:00Dev Biol. 2009 Aug 1;332(1):25-35. doi: 10.1016/j.ydbio.2009.05.542. Epub 2009 May 9.

}, month = {Aug 1}, pages = {25-35}, abstract = {

The importance of regulatory evolution to the diversification of plant morphology is well recognized. Some of the best-understood examples also involve gene duplication and co-option of deeply conserved genetic modules. These instances underscore the important role of gene duplication events, which are associated with regulatory sub- and neofunctionalization. In particular, we discuss the relationship between regulatory evolution following gene duplication and the evolution of floral novelty. We also consider the repeated co-option of TCP gene family members to promote aspects of floral symmetry and the KNOX/ARP meristem genetic module to control compound leaf development. Both of these patterns of genetic convergence involve modifications of an ancestral regulatory network to create novel expression domains. Overall, such examples highlight the interdependence of the three processes--regulatory evolution, gene duplication and co-option--within the context of plant developmental evolution.

}, keywords = {*Evolution, Molecular, *Gene Expression Regulation, Plant, *Gene Regulatory Networks, Gene Duplication, Plant Leaves/anatomy \& histology/genetics, Plants/*anatomy \& histology/*genetics}, isbn = {1095-564X (Electronic)0012-1606 (Linking)}, author = {Rosin, F. M. and Kramer, E. M.} } @article {592001, title = {One size fits all? Molecular evidence for a commonly inherited petal identity program in Ranunculales}, journal = {Am J Bot}, volume = {96}, number = {1}, year = {2009}, note = {

Rasmussen, David AKramer, Elena MZimmer, Elizabeth Aeng2009/01/01 00:00Am J Bot. 2009 Jan;96(1):96-109. doi: 10.3732/ajb.0800038. Epub 2008 Dec 19.

}, month = {Jan}, pages = {96-109}, abstract = {

Petaloid organs are a major component of the floral diversity observed across nearly all major clades of angiosperms. The variable morphology and development of these organs has led to the hypothesis that they are not homologous but, rather, have evolved multiple times. A particularly notable example of petal diversity, and potential homoplasy, is found within the order Ranunculales, exemplified by families such as Ranunculaceae, Berberidaceae, and Papaveraceae. To investigate the molecular basis of petal identity in Ranunculales, we used a combination of molecular phylogenetics and gene expression analysis to characterize APETALA3 (AP3) and PISTILLATA (PI) homologs from a total of 13 representative genera of the order. One of the most striking results of this study is that expression of orthologs of a single AP3 lineage is consistently petal-specific across both Ranunculaceae and Berberidaceae. We conclude from this finding that these supposedly homoplastic petals in fact share a developmental genetic program that appears to have been present in the common ancestor of the two families. We discuss the implications of this type of molecular data for long-held typological definitions of petals and, more broadly, the evolution of petaloid organs across the angiosperms.

}, isbn = {0002-9122 (Print)0002-9122 (Linking)}, author = {Rasmussen, D. A. and Kramer, E. M. and Zimmer, E. A.} } @article {592056, title = {Are we there yet? Tracking the development of new model systems}, journal = {Trends Genet}, volume = {24}, number = {7}, year = {2008}, note = {

Abzhanov, ArhatExtavour, Cassandra GGroover, AndrewHodges, Scott AHoekstra, Hopi EKramer, Elena MMonteiro, AntoniaengReviewEngland2008/06/03 09:00Trends Genet. 2008 Jul;24(7):353-60. doi: 10.1016/j.tig.2008.04.002.

}, month = {Jul}, pages = {353-60}, abstract = {

It is increasingly clear that additional {\textquoteright}model{\textquoteright} systems are needed to elucidate the genetic and developmental basis of organismal diversity. Whereas model system development previously required enormous investment, recent advances including the decreasing cost of DNA sequencing and the power of reverse genetics to study gene function are greatly facilitating the process. In this review, we consider two aspects of the development of new genetic model systems: first, the types of questions being advanced using these new models; and second, the essential characteristics and molecular tools for new models, depending on the research focus. We hope that researchers will be inspired to explore this array of emerging models and even consider developing new molecular tools for their own favorite organism.

}, keywords = {*Models, Biological, *Models, Genetic, Animals, Research}, isbn = {0168-9525 (Print)0168-9525 (Linking)}, author = {Abzhanov, A. and Extavour, C. G. and Groover, A. and Hodges, S. A. and Hoekstra, HE and Kramer, E. M. and Monteiro, A.} } @article {592051, title = {Variation and constraint in plant evolution and development}, journal = {Heredity (Edinb)}, volume = {100}, number = {2}, year = {2008}, note = {

Kalisz, SKramer, E MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ReviewEngland2007/02/03 09:00Heredity (Edinb). 2008 Feb;100(2):171-7. Epub 2007 Jan 31.

}, month = {Feb}, pages = {171-7}, abstract = {

The goal of this short review is to consider the interrelated phenomena of phenotypic variation and genetic constraint with respect to plant diversity. The unique aspects of plants, including sessile habit, modular growth and diverse developmental programs expressed at the phytomer level, merit a specific examination of the genetic basis of their phenotypic variation, and how they experience and escape genetic constraint. Numerous QTL studies with wild and domesticated plants reveal that most phenotypic traits are polygenic but vary in the number and effect of the loci contributing, from a few loci of large effects to many with small effects. Further, somatic mutations, developmental plasticity and epigenetic variation, especially gene methylation, can contribute to increases in phenotypic variation. The flip side of these processes, genetic constraint, can similarly be the result of many factors, including pleiotropy, canalization and genetic redundancy. Genetic constraint is not only a mechanism to prevent change, however, it can also serve to direct evolution along certain paths. Ultimately, genetic constraint often comes full circle and is released through events such as hybridization, genome duplication and epigenetic remodeling. We are just beginning to understand how these processes can operate simultaneously during the evolution of ecologically important traits in plants.

}, keywords = {*Biological Evolution, *Genetic Variation, Epistasis, Genetic, Phenotype, Plants/*genetics, Quantitative Trait Loci}, isbn = {1365-2540 (Electronic)0018-067X (Linking)}, author = {Kalisz, S. and Kramer, E. M.} } @article {592076, title = {Columbines}, journal = {Curr Biol}, volume = {17}, number = {23}, year = {2007}, note = {

Hodges, Scott AKramer, Elena MengReviewEngland2007/12/07 09:00Curr Biol. 2007 Dec 4;17(23):R992-4.

}, month = {Dec 4}, pages = {R992-4}, keywords = {*Aquilegia/classification/genetics/growth \& development, Biological Evolution, Flowers/physiology, Genome, Plant, Species Specificity}, isbn = {0960-9822 (Print)0960-9822 (Linking)}, author = {Hodges, S. A. and Kramer, E. M.} } @article {592061, title = {Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia}, journal = {Plant Cell}, volume = {19}, number = {3}, year = {2007}, note = {

Kramer, Elena MHolappa, LynnGould, BillieJaramillo, M AlejandraSetnikov, DimitriySantiago, Philip MengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2007/04/03 09:00Plant Cell. 2007 Mar;19(3):750-66. Epub 2007 Mar 30.

}, month = {Mar}, pages = {750-66}, abstract = {

The basal eudicot Aquilegia (columbine) has an unusual floral structure that includes two morphologically distinct whorls of petaloid organs and a clearly differentiated fifth organ type, the staminodium. In this study, we have sought to determine how Aquilegia homologs of the B class genes APETALA3 (AP3) and PISTILLATA (PI) contribute to these novel forms of organ identity. Detailed expression analyses of the three AP3 paralogs and one PI homolog in wild-type and floral homeotic mutant lines reveal complex patterns that suggest that canonical B class function has been elaborated in Aquilegia. Yeast two-hybrid studies demonstrate that the protein products of Aquilegia{\textquoteright}s AP3 and PI homologs can form heterodimers, much like what has been observed for their core eudicot homologs. Downregulation of AqvPI using virus-induced gene silencing indicates that in addition to petal and stamen identity, this locus is essential to staminodial identity but may not control the identity of the petaloid sepals. Our findings show that preexisting floral organ identity programs can be partitioned and modified to produce additional organ types. In addition, they indicate that some types of petaloid organs are not entirely dependent on AP3/PI homologs for their identity.

}, keywords = {*Genes, Plant, Aquilegia/*anatomy \& histology/*genetics/growth \& development/ultrastructure, Flowers/cytology/*genetics/growth \& development/ultrastructure, Gene Expression Profiling, Gene Expression Regulation, Plant, Gene Silencing, In Situ Hybridization, Meristem/cytology, Models, Biological, Molecular Sequence Data, Mutation/genetics, Phenotype, Plant Proteins/genetics/*metabolism, Protein Binding, RNA, Messenger/genetics/metabolism, Sequence Homology, Amino Acid, Two-Hybrid System Techniques}, isbn = {1040-4651 (Print)1040-4651 (Linking)}, author = {Kramer, E. M. and Holappa, L. and Gould, B. and Jaramillo, M. A. and Setnikov, D. and Santiago, P. M.} } @article {592071, title = {Molecular evolution of the petal and stamen identity genes, APETALA3 and PISTILLATA, after petal loss in the Piperales}, journal = {Mol Phylogenet Evol}, volume = {44}, number = {2}, year = {2007}, note = {

Jaramillo, M AlejandraKramer, Elena MengResearch Support, Non-U.S. Gov{\textquoteright}t2007/06/20 09:00Mol Phylogenet Evol. 2007 Aug;44(2):598-609. Epub 2007 Apr 4.

}, month = {Aug}, pages = {598-609}, abstract = {

Organ loss is an evolutionary phenomenon commonly observed in all kinds of multicellular organisms. Across the angiosperms, petals have been lost several times over the course of their diversification. We examined the evolution of petal and stamen identity genes in the Piperales, a basal lineage of angiosperms that includes the perianthless (with no petals or sepals) families Piperaceae and Saururaceae as well as the Aristolochiaceae, which exhibit a well-developed perianth. Here, we provide evidence for relaxation of selection on the putative petal and stamen identity genes, homologs of APETALA3 and PISTILLATA, following the loss of petals in the Piperales. Our results are particularly interesting as the B-class genes are not only responsible for the production of petals but are also central to stamen identity, the male reproductive organs that show no modification in these plants. Relaxed purifying selection after the loss of only one of these organs suggests that there has been dissociation of the functional roles of these genes in the Piperales.

}, keywords = {*Evolution, Molecular, Amino Acid Sequence, Angiosperms/anatomy \& histology/classification/*genetics, Arabidopsis/anatomy \& histology/classification/genetics, Aristolochia/anatomy \& histology/classification/genetics, Conserved Sequence, Flowers/anatomy \& histology/classification/*genetics, Genes, Plant/*genetics, MADS Domain Proteins/chemistry/classification/*genetics, Molecular Sequence Data, Phylogeny, Sequence Alignment}, isbn = {1055-7903 (Print)1055-7903 (Linking)}, author = {Jaramillo, M. A. and Kramer, E. M.} } @article {592081, title = {Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae)}, journal = {Plant Methods}, volume = {3}, year = {2007}, note = {

Gould, BillieKramer, Elena MengEngland2007/04/14 09:00Plant Methods. 2007 Apr 12;3:6.

}, pages = {6}, abstract = {

BACKGROUND: The lower eudicot genus Aquilegia, commonly known as columbine, is currently the subject of extensive genetic and genomic research aimed at developing this taxon as a new model for the study of ecology and evolution. The ability to perform functional genetic analyses is a critical component of this development process and ultimately has the potential to provide insight into the genetic basis for the evolution of a wide array of traits that differentiate flowering plants. Aquilegia is of particular interest due to both its recent evolutionary history, which involves a rapid adaptive radiation, and its intermediate phylogenetic position between core eudicot (e.g., Arabidopsis) and grass (e.g., Oryza) model species. RESULTS: Here we demonstrate the effective use of a reverse genetic technique, virus-induced gene silencing (VIGS), to study gene function in this emerging model plant. Using Agrobacterium mediated transfer of tobacco rattle virus (TRV) based vectors, we induce silencing of PHYTOENE DESATURASE (AqPDS) in Aquilegia vulgaris seedlings, and ANTHOCYANIDIN SYNTHASE (AqANS) and the B-class floral organ identity gene PISTILLATA in A. vulgaris flowers. For all of these genes, silencing phenotypes are associated with consistent reduction in endogenous transcript levels. In addition, we show that silencing of AqANS has no effect on overall floral morphology and is therefore a suitable marker for the identification of silenced flowers in dual-locus silencing experiments. CONCLUSION: Our results show that TRV-VIGS in Aquilegia vulgaris allows data to be rapidly obtained and can be reproduced with effective survival and silencing rates. Furthermore, this method can successfully be used to evaluate the function of early-acting developmental genes. In the future, data derived from VIGS analyses will be combined with large-scale sequencing and microarray experiments already underway in order to address both recent and ancient evolutionary questions.

}, isbn = {1746-4811 (Electronic)1746-4811 (Linking)}, author = {Gould, B. and Kramer, E. M.} } @article {592091, title = {Evolution. Traversing the adaptive landscape in snapdragons}, journal = {Science}, volume = {313}, number = {5789}, year = {2006}, note = {

Kramer, Elena MDonohue, KathleenengCommentNew York, N.Y.2006/08/19 09:00Science. 2006 Aug 18;313(5789):924-5.

}, month = {Aug 18}, pages = {924-5}, keywords = {*Adaptation, Biological, *Biological Evolution, *Genetic Speciation, Alleles, Antirrhinum/*genetics, Flowers/*genetics, Genes, Plant, Genotype, Hybridization, Genetic, Models, Genetic, Phenotype, Pigmentation/*genetics, Selection, Genetic}, isbn = {1095-9203 (Electronic)0036-8075 (Linking)}, author = {Kramer, E. M. and Donohue, K.} } @article {592086, title = {A simplified explanation for the frameshift mutation that created a novel C-terminal motif in the APETALA3 gene lineage}, journal = {BMC Evol Biol}, volume = {6}, year = {2006}, note = {

Kramer, Elena MSu, Huei-JiunWu, Cheng-ChiangHu, Jer-MingengResearch Support, Non-U.S. Gov{\textquoteright}tEngland2006/03/28 09:00BMC Evol Biol. 2006 Mar 24;6:30.

}, pages = {30}, abstract = {

BACKGROUND: The evolution of type II MADS box genes has been extensively studied in angiosperms. One of the best-understood subfamilies is that of the Arabidopsis gene APETALA3 (AP3). Previous work has demonstrated that the ancestral paleoAP3 lineage was duplicated at some point within the basal eudicots to give rise to the paralogous TM6 and euAP3 lineages. This event was followed in euAP3 orthologs by the replacement of the C-terminal paleoAP3 motif with the derived euAP3 motif. It has been suggested that the new motif was created by an eight-nucleotide insertion that produced a translational frameshift. RESULTS: The addition of 25 eudicot AP3 homologs to the existing dataset has allowed us to clarify the process by which the euAP3 motif evolved. Phylogenetic analysis indicates that the euAP3/TM6 duplication maps very close to the base of the core eudicots, associated with the families Trochodendraceae and Buxaceae. We demonstrate that although the transformation of paleoAP3 into euAP3 was due to a frameshift mutation, this was the result of a single nucleotide deletion. The use of ancestral character state reconstructions has allowed us to demonstrate that the frameshift was accompanied by few other nucleotide changes. We further confirm that the sequence is evolving as coding region. CONCLUSION: This study demonstrates that the simplest of genetic changes can result in the remodeling of protein sequence to produce a kind of molecular {\textquoteright}hopeful monster.{\textquoteright} Moreover, such a novel protein motif can become conserved almost immediately on the basis of what appears to be a rapidly generated new function. Given that the existing data on the function of such C-terminal motifs are somewhat disparate and contradictory, we have sought to synthesize previous findings within the context of the current analysis and thereby highlight specific hypotheses that require further investigation before the significance of the euAP3 frameshift event can be fully understood.

}, keywords = {Amino Acid Sequence, Arabidopsis Proteins/*chemistry/*genetics, Base Sequence, Conserved Sequence, Frameshift Mutation/*genetics, MADS Domain Proteins/*chemistry/*genetics, Phylogeny, Plants/*genetics, Polymorphism, Single Nucleotide}, isbn = {1471-2148 (Electronic)1471-2148 (Linking)}, author = {Kramer, E. M. and Su, H. J. and Wu, C. C. and Hu, J. M.} } @article {592116, title = {Evolutionary dynamics of genes controlling floral development}, journal = {Curr Opin Plant Biol}, volume = {8}, number = {1}, year = {2005}, note = {

Kramer, Elena MHall, Jocelyn CengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Review2005/01/18 09:00Curr Opin Plant Biol. 2005 Feb;8(1):13-8.

}, month = {Feb}, pages = {13-8}, abstract = {

Advances in the understanding of floral developmental genetics in model species such as Arabidopsis continue to provide an important foundation for comparative studies in other flowering plants. In particular, floral organ identity genes are the focus of many projects that are addressing both ancient and recent evolutionary questions. Expanded analyses of the evolution of these gene lineages have highlighted the dynamic nature of the gene birth-and-death process, and may have significant implications for the evolution of genetic pathways. Crucial functional studies of floral organ identity genes in diverse taxa are allowing the first real insight into the conservation of gene function, while findings on the genetic control of organ elaboration offer to open up new avenues for investigation. Taken together, these trends show that the field of floral developmental evolution continues to make significant progress towards elucidating the processes that have shaped the evolution of flower development and morphology.

}, keywords = {*Evolution, Molecular, Angiosperms/*genetics/growth \& development, Flowers/*genetics/growth \& development, Gene Expression Regulation, Developmental/genetics, Gene Expression Regulation, Plant/genetics, Genes, Plant/physiology}, isbn = {1369-5266 (Print)1369-5266 (Linking)}, author = {Kramer, E. M. and Hall, J. C.} } @article {592126, title = {Floral MADS box genes and homeotic gender dimorphism in Thalictrum dioicum (Ranunculaceae) - a new model for the study of dioecy}, journal = {Plant J}, volume = {41}, number = {5}, year = {2005}, note = {

Di Stilio, Veronica SKramer, Elena MBaum, David AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2005/02/11 09:00Plant J. 2005 Mar;41(5):755-66.

}, month = {Mar}, pages = {755-66}, abstract = {

In most dioecious angiosperm species, flowers are initially perfect but abort either stamens or carpels during their development, indicating that sex determination occurs after floral organ identity has been established. Dioecious members of the genus Thalictrum (meadow-rue), however, produce flowers that lack aborted organs. Examination of early flower development of T. dioicum confirms that flowers are male or female from inception, raising the possibility that genetic mechanisms working at or above the level of organ identity promote sex determination through a homeotic-like mechanism. In order to investigate this possibility, we identified homologs of the organ identity genes PISTILLATA (PI), APETALA3 (AP3) and AGAMOUS (AG) from T. dioicum and the hermaphroditic species T. thalictroides. A combination of early and late duplication events was uncovered in these gene lineages and expression analyses indicate that these events are generally associated with divergence in gene regulation. In light of these findings, we discuss the potential of T. dioicum as a new model for the study of sex determination in the basal eudicots.

}, keywords = {Amino Acid Sequence, Flowers/*genetics/ultrastructure, MADS Domain Proteins/*genetics, Microscopy, Electron, Scanning, Models, Genetic, Molecular Sequence Data, Phylogeny, Plant Proteins/*genetics, Ranunculaceae/classification/*genetics, Sequence Alignment, Sequence Homology, Amino Acid}, isbn = {0960-7412 (Print)0960-7412 (Linking)}, author = {Di Stilio, V. S. and Kramer, E. M. and Baum, D.A.} } @article {592111, title = {Genetic basis for innovations in floral organ identity}, journal = {J Exp Zool B Mol Dev Evol}, volume = {304}, number = {6}, year = {2005}, note = {

Kramer, Elena MJaramillo, M AlejandraengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2005/05/10 09:00J Exp Zool B Mol Dev Evol. 2005 Nov 15;304(6):526-35.

}, month = {Nov 15}, pages = {526-35}, abstract = {

Of the many innovations associated with the radiation of the angiosperms, the evolution of a petal identity program is among the best understood from a genetic standpoint. Although the existing data do indicate that similar genetic mechanisms control petal development across diverse taxa, there is also considerable evidence for variability in petal identity programs, likely due to a number of factors. These points are illustrated through a review of our current knowledge on the subject, integrating phylogenetic, morphological, and genetic studies. Comparative studies of petal identity highlight the complex nature of homology in plants and stand as a cautionary tale for the interpretation of gene expression data.

}, keywords = {*Biological Evolution, Flowers/*anatomy \& histology/*genetics/growth \& development, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genetic Variation, Models, Biological, Morphogenesis}, isbn = {1552-5007 (Print)1552-5007 (Linking)}, author = {Kramer, E. M. and Jaramillo, M. A.} } @article {592121, title = {Methods for studying the evolution of plant reproductive structures: comparative gene expression techniques}, journal = {Methods Enzymol}, volume = {395}, year = {2005}, note = {

Kramer, Elena MengComparative Study2005/05/04 09:00Methods Enzymol. 2005;395:617-36.

}, pages = {617-36}, abstract = {

A major component of evolutionary developmental (evo-devo) genetics is the analysis of gene expression patterns in nonmodel species. This comparative approach can take many forms, including reverse-transcriptase polymerase chain reaction, Northern blot hybridization, and in situ hybridization. The choice of technique depends on several issues such as the availability of fresh tissue, as well as the expected expression level and pattern of the candidate gene in question. Although the protocols for these procedures are fairly standard, optimization is often required because of the specific characteristics of the species under analysis. This chapter describes several methods commonly used to determine gene expression patterns in angiosperms, particularly in floral tissues. Suggestions for adapting basic protocols for diverse taxa and troubleshooting are also extensively discussed.

}, keywords = {*Gene Expression, *Genetic Techniques, Biological Evolution, Blotting, Northern/methods, Genes, Plant, Histological Techniques, In Situ Hybridization/methods, Plant Physiological Phenomena, Plants/anatomy \& histology/*genetics, Polymerase Chain Reaction/methods, Reproduction, RNA Probes, RNA, Plant/genetics/isolation \& purification}, isbn = {0076-6879 (Print)0076-6879 (Linking)}, author = {Kramer, E. M.} } @article {592146, title = {APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth of Aristolochia (Aristolochiaceae)}, journal = {Evol Dev}, volume = {6}, number = {6}, year = {2004}, note = {

Jaramillo, M AlejandraKramer, Elena MengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.2004/10/29 09:00Evol Dev. 2004 Nov-Dec;6(6):449-58.

}, month = {Nov-Dec}, pages = {449-58}, abstract = {

Several lines of evidence suggest that sterile floral organs, collectively known as the perianth, have evolved multiple times during the evolution of the angiosperms. In the family Aristolochiaceae, the perianth is formed by two whorls of organs in the genus Saruma but by only one whorl in the remaining genera, including Aristolochia. Although the morphology of Saruma is similar in appearance to the core eudicot perianth, with leaf-like sepals and showy colored petals, the unipartite perianth of Aristolochia combines morphological aspects of both calyx and corolla. To investigate the organ identity program functioning in the novel perianth of Aristolochia, we identified homologs of the B-class genes APETALA3 (AP3) and PISTILLATA (PI) in both Saruma and Aristolochia. The expression patterns of these genes in Saruma indicate they are functioning in the development of the second whorl petaloid organs and third whorl stamens. In Aristolochia, however, the expression of AP3 and PI homologs in the perianth does not suggest a role in organ identity but, rather, in promoting late aspects of cell differentiation. The implications of these findings for the evolution of both petaloidy and B gene function are discussed.

}, keywords = {Arabidopsis Proteins/*biosynthesis/genetics, Aristolochia/genetics/*physiology, Biological Evolution, Flowers/genetics/*physiology/ultrastructure, Gene Expression Regulation, Plant/genetics/*physiology, MADS Domain Proteins/*biosynthesis/genetics, Plant Epidermis/genetics/*physiology/ultrastructure, Plant Proteins/*biosynthesis/genetics, Reproduction/genetics/physiology, Sequence Homology, Amino Acid}, isbn = {1520-541X (Print)1520-541X (Linking)}, author = {Jaramillo, M. A. and Kramer, E. M.} } @article {592131, title = {Evolution of the APETALA3 and PISTILLATA lineages of MADS-box-containing genes in the basal angiosperms}, journal = {Mol Biol Evol}, volume = {21}, number = {3}, year = {2004}, note = {

Stellari, Giulia MJaramillo, M AlejandraKramer, Elena MengResearch Support, Non-U.S. Gov{\textquoteright}t2003/12/25 05:00Mol Biol Evol. 2004 Mar;21(3):506-19. Epub 2003 Dec 23.

}, month = {Mar}, pages = {506-19}, abstract = {

The B class genes, including homologs of the Arabidopsis loci APETALA3 (AP3) and PISTILLATA (PI ), appear to play a conserved role in the determination of petal and stamen identity across core eudicot angiosperms. Understanding how and when these functions evolved is a critical component of elucidating the evolution of flowers, particularly the appearance of petaloid perianth organs. Before comparisons of gene expression patterns or functions can be made, however, it is necessary to establish the orthology of AP3 and PI homologs from basal angiosperms. Here, we report the identification and analysis of 29 new representatives of the B gene lineage from basal ANITA and magnoliid dicot angiosperms. These studies indicate that gene duplications have occurred at every phylogenetic level, both before and after the duplication that produced the separate AP3 and PI lineages. Comparison of genomic structure among PI homologs indicates that a 12-nucleotide deletion that had been considered synapomorphic for the whole PI lineage actually arose within the ANITA grade, after the split of the Nymphaeales but before the separation of the Austrobaileyales. Evidence for alternative splicing of the Nymphaea AP3 homolog is also presented. The implications of these findings for angiosperm systematics, the conservation of AP3 and PI gene function, and the evolution of the ABC program are discussed.

}, keywords = {*Evolution, Molecular, Alternative Splicing, Amino Acid Sequence, Angiosperms/classification/*genetics, Arabidopsis Proteins/*genetics, Arabidopsis/genetics, Base Sequence, Consensus Sequence, MADS Domain Proteins/*genetics/metabolism, Molecular Sequence Data, Multigene Family, Phylogeny, Sequence Homology, Amino Acid}, isbn = {0737-4038 (Print)0737-4038 (Linking)}, author = {Stellari, G. M. and Jaramillo, M. A. and Kramer, E. M.} } @article {592136, title = {Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms}, journal = {Genetics}, volume = {166}, number = {2}, year = {2004}, note = {

Kramer, Elena MJaramillo, M AlejandraDi Stilio, Veronica SengResearch Support, Non-U.S. Gov{\textquoteright}t2004/03/17 05:00Genetics. 2004 Feb;166(2):1011-23.

}, month = {Feb}, pages = {1011-23}, abstract = {

Members of the AGAMOUS (AG) subfamily of MIKC-type MADS-box genes appear to control the development of reproductive organs in both gymnosperms and angiosperms. To understand the evolution of this subfamily in the flowering plants, we have identified 26 new AG-like genes from 15 diverse angiosperm species. Phylogenetic analyses of these genes within a large data set of AG-like sequences show that ancient gene duplications were critical in shaping the evolution of the subfamily. Before the radiation of extant angiosperms, one event produced the ovule-specific D lineage and the well-characterized C lineage, whose members typically promote stamen and carpel identity as well as floral meristem determinacy. Subsequent duplications in the C lineage resulted in independent instances of paralog subfunctionalization and maintained functional redundancy. Most notably, the functional homologs AG from Arabidopsis and PLENA (PLE) from Antirrhinum are shown to be representatives of separate paralogous lineages rather than simple genetic orthologs. The multiple subfunctionalization events that have occurred in this subfamily highlight the potential for gene duplication to lead to dissociation among genetic modules, thereby allowing an increase in morphological diversity.

}, keywords = {*Evolution, Molecular, *Gene Duplication, *Multigene Family, Amino Acid Sequence, Angiosperms/*genetics, MADS Domain Proteins/*genetics, Molecular Sequence Data, Phylogeny}, isbn = {0016-6731 (Print)0016-6731 (Linking)}, author = {Kramer, E. M. and Jaramillo, M. A. and Di Stilio, V. S.} } @article {592156, title = {Differential regulation of symmetry genes and the evolution of floral morphologies}, journal = {Proc Natl Acad Sci USA}, volume = {100}, number = {22}, year = {2003}, note = {

Hileman, Lena CKramer, Elena MBaum, David AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2003/10/14 05:00Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12814-9. Epub 2003 Oct 10.

}, month = {Oct 28}, pages = {12814-9}, abstract = {

Shifts in flower symmetry have occurred frequently during the diversification of angiosperms, and it is thought that such shifts play important roles in plant-pollinator interactions. In the model developmental system Antirrhinum majus (snapdragon), the closely related genes CYCLOIDEA (CYC) and DICHOTOMA (DICH) are needed for the development of zygomorphic flowers and the determination of adaxial (dorsal) identity of floral organs, including adaxial stamen abortion and asymmetry of adaxial petals. However, it is not known whether these genes played a role in the divergence of species differing in flower morphology and pollination mode. We compared A. majus with a close relative, Mohavea confertiflora (desert ghost flower), which differs from Antirrhinum in corolla (petal) symmetry and pollination mode. In addition, Mohavea has undergone a homeotic-like transformation in stamen number relative to Antirrhinum, aborting the lateral and adaxial stamens during flower development. Here we show that the patterns of expression of CYC and DICH orthologs have shifted in concert with changes in floral morphology. Specifically, lateral stamen abortion in Mohavea is correlated with an expansion of CYC and DICH expression, and internal symmetry of Mohavea adaxial petals is correlated with a reduction in DICH expression during petal differentiation. We propose that changes in the pattern of CYC and DICH expression have contributed to the derived flower morphology of Mohavea and may reflect adaptations to a pollination strategy resulting from a mimetic relationship, linking the genetic basis for morphological evolution to the ecological context in which the morphology arose.

}, keywords = {*Gene Expression Regulation, Plant, *Genes, Plant, *Phylogeny, Antirrhinum/*classification/*genetics, Biological Evolution, Flowers/*genetics, In Situ Hybridization, Molecular Sequence Data, Reverse Transcriptase Polymerase Chain Reaction, RNA, Messenger/genetics, RNA, Plant/genetics}, isbn = {0027-8424 (Print)0027-8424 (Linking)}, author = {Hileman, L. C. and Kramer, E. M. and Baum, D.A.} } @article {592171, title = {Evolution of genetic mechanisms controlling petal development}, journal = {Nature}, volume = {399}, number = {6732}, year = {1999}, note = {

Kramer, E MIrish, V FengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ENGLAND1999/05/21 06:00Nature. 1999 May 13;399(6732):144-8.

}, month = {May 13}, pages = {144-8}, abstract = {

Molecular genetic studies in Arabidopsis thaliana and other higher-eudicot flowering plants have led to the development of the {\textquoteright}ABC{\textquoteright} model of the determination of organ identity in flowers, in which three classes of gene, A, B and C, are thought to work together to determine organ identity. According to this model, the B-class genes APETALA3 (AP3) and PISTILLATA (PI) act to specify petal and stamen identity. Here we test whether the roles of these genes are conserved throughout the angiosperms by analysing the expression of AP3 and PI orthologues in the lower eudicot subclass Ranunculidae. We show that, although expression of these orthologues in the stamens is conserved, the expression patterns in the petals differ from those found in the higher eudicots. The differences between these expression patterns suggest that the function of AP3 and PI homologues as B-class organ-identity genes is not rigidly conserved among all angiosperms. These observations have important implications for understanding the evolution of both angiosperm petals and the genetic mechanisms that control the identities of floral organs.

}, keywords = {*Arabidopsis Proteins, *Evolution, Molecular, *Genes, Plant, *MADS Domain Proteins, Angiosperms/classification/*genetics/growth \& development, Arabidopsis/genetics/growth \& development, Blotting, Northern, Blotting, Southern, Cloning, Molecular, Gene Expression, Homeodomain Proteins/genetics, Models, Biological, Molecular Sequence Data, Phylogeny, Plant Structures/growth \& development, Transcription Factors/genetics}, isbn = {0028-0836 (Print)0028-0836 (Linking)}, author = {Kramer, E. M. and Irish, V. F.} } @article {592176, title = {Courtship and visual defects of cacophony mutants reveal functional complexity of a calcium-channel alpha1 subunit in Drosophila}, journal = {Genetics}, volume = {149}, number = {3}, year = {1998}, note = {

Smith, L APeixoto, A AKramer, E MVillella, AHall, J CengGM-21473/GM/NIGMS NIH HHS/Research Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.1998/07/03Genetics. 1998 Jul;149(3):1407-26.

}, month = {Jul}, pages = {1407-26}, abstract = {

We show by molecular analysis of behavioral and physiological mutants that the Drosophila Dmca1A calcium-channel alpha1 subunit is encoded by the cacophony (cac) gene and that nightblind-A and lethal(1)L13 mutations are allelic to cac with respect to an expanded array of behavioral and physiological phenotypes associated with this gene. The cacS mutant, which exhibits defects in the patterning of courtship lovesong and a newly revealed but subtle abnormality in visual physiology, is mutated such that a highly conserved phenylalanine (in one of the quasi-homologous intrapolypeptide regions called IIIS6) is replaced by isoleucine. The cacH18 mutant exhibits defects in visual physiology (including complete unresponsiveness to light in certain genetic combinations) and visually mediated behaviors; this mutant (originally nbAH18) has a stop codon in an alternative exon (within the cac ORF), which is differentially expressed in the eye. Analysis of the various courtship and visual phenotypes associated with this array of cac mutants demonstrates that Dmca1A calcium channels mediate multiple, separable biological functions; these correlate in part with transcript diversity generated via alternative splicing.

}, keywords = {*Mutation, *Sexual Behavior, Animal, Alleles, Amino Acid Sequence, Animals, Calcium Channels/biosynthesis/chemistry/*genetics, Chromosome Mapping, Drosophila/genetics/*physiology, Electroretinography, Female, Genes, Insect, Genes, Lethal, Genetic Variation, Macromolecular Substances, Male, Molecular Sequence Data, Night Blindness/genetics, Polymerase Chain Reaction, Psychomotor Performance, Sequence Alignment, Sequence Homology, Amino Acid, Vision Disorders/*genetics, X Chromosome}, isbn = {0016-6731 (Print)0016-6731 (Linking)}, author = {Smith, L. A. and Peixoto, A. A. and Kramer, E. M. and Villella, A. and Hall, J. C.} } @article {592181, title = {Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages}, journal = {Genetics}, volume = {149}, number = {2}, year = {1998}, note = {

Kramer, E MDorit, R LIrish, V FengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.1998/06/11Genetics. 1998 Jun;149(2):765-83.

}, month = {Jun}, pages = {765-83}, abstract = {

The specification of floral organ identity in the higher dicots depends on the function of a limited set of homeotic genes, many of them members of the MADS-box gene family. Two such genes, APETALA3 (AP3) and PISTILLATA (PI), are required for petal and stamen identity in Arabidopsis; their orthologs in Antirrhinum exhibit similar functions. To understand how changes in these genes may have influenced the morphological evolution of petals and stamens, we have cloned twenty-six homologs of the AP3 and PI genes from two higher eudicot and eleven lower eudicot and magnolid dicot species. The sequences of these genes reveal the presence of characteristic PI- and AP3-specific motifs. While the PI-specific motif is found in all of the PI genes characterized to date, the lower eudicot and magnolid dicot AP3 homologs contain distinctly different motifs from those seen in the higher eudicots. An analysis of all the available AP3 and PI sequences uncovers multiple duplication events within each of the two gene lineages. A major duplication event in the AP3 lineage coincides with the base of the higher eudicot radiation and may reflect the evolution of a petal-specific AP3 function in the higher eudicot lineage.

}, keywords = {*Arabidopsis Proteins, *Evolution, Molecular, *Genes, Plant, *MADS Domain Proteins, *Multigene Family, Amino Acid Sequence, Homeodomain Proteins/*genetics, Lycopersicon esculentum/genetics, Molecular Sequence Data, Papaver/genetics, Phylogeny, Plant Proteins/*genetics, Plant Structures/*genetics/*growth \& development, Plants, Medicinal, Sequence Alignment, Sequence Analysis, DNA, Sequence Homology, Amino Acid, Transcription Factors/*genetics}, isbn = {0016-6731 (Print)0016-6731 (Linking)}, author = {Kramer, E. M. and Dorit, R. L. and Irish, V. F.} }