Pleiotropy, redundancy and the evolution of flowers.

Most angiosperm flowers are tightly integrated, functionally bisexual shoots that have carpels with enclosed ovules. Flowering plants evolved from within the gymnosperms, which lack this combination of innovations. Paradoxically, phylogenetic reconstructions suggest that the flowering plant lineage substantially pre-dates the evolution of flowers themselves. We provide a model based on known gene regulatory networks whereby positive selection on a single, partially redundant gene duplicate 'trapped' the ancestors of flower-bearing plants into the condensed, bisexual state approximately 130 million years ago. The LEAFY (LFY) gene of Arabidopsis encodes a master regulator that functions as the main conduit of environmental signals to the reproductive developmental program. We directly link the elimination of one LFY paralog, pleiotropically maintained in gymnosperms, to the sudden appearance of flowers in the fossil record.

[1]  E. M. Friis,et al.  Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous , 2001, Nature.

[2]  K. Norstog,et al.  The Biology of the Cycads , 2020 .

[3]  Victor A. Albert,et al.  Ontogenetic Systematics, Molecular Developmental Genetics, and the Angiosperm Petal , 1998 .

[4]  D. Weigel,et al.  Integration of floral inductive signals in Arabidopsis , 2000, Nature.

[5]  J. Palmer,et al.  Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  C. Ainsworth,et al.  Boys and Girls Come Out to Play: The Molecular Biology of Dioecious Plants , 2000 .

[7]  M. Sanderson,et al.  Error, bias, and long-branch attraction in data for two chloroplast photosystem genes in seed plants. , 2000, Molecular biology and evolution.

[8]  K. Sakakibara,et al.  Characterization of a FLORICAULA/LEAFY Homologue of Gnetum parvifolium and Its Implications for the Evolution of Reproductive Organs in Seed Plants , 2001, International Journal of Plant Sciences.

[9]  D. Weigel,et al.  A Molecular Link between Stem Cell Regulation and Floral Patterning in Arabidopsis , 2001, Cell.

[10]  J. Doyle Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. , 1998, Molecular phylogenetics and evolution.

[11]  S. Dellaporta,et al.  Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion , 1993, Cell.

[12]  P. K. Endress Structure and Function of Female and Bisexual Organ Complexes in Gnetales , 1996, International Journal of Plant Sciences.

[13]  H. Saedler,et al.  MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Weigel,et al.  LEAFY controls floral meristem identity in Arabidopsis , 1992, Cell.

[15]  D. Weigel,et al.  Evolution of floral meristem identity genes. Analysis of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. , 2001, Plant physiology.

[16]  B. Fowler,et al.  NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Källersjö,et al.  Seed Plant Relationships and the Systematic Position of Gnetales Based on Nuclear and Chloroplast DNA: Conflicting Data, Rooting Problems, and the Monophyly of Conifers , 2002, International Journal of Plant Sciences.

[18]  D. S. Parker,et al.  The Mostly Male Theory of Flower Evolutionary Origins: from Genes to Fossils , 2000 .

[19]  E. Coen,et al.  The war of the whorls: genetic interactions controlling flower development , 1991, Nature.

[20]  E. Mellerowicz,et al.  PRFLL– a Pinus radiata homologue of FLORICAULA and LEAFY is expressed in buds containing vegetative shoot and undifferentiated male cone primordia , 1998, Planta.

[21]  D Weigel,et al.  LEAFY expression and flower initiation in Arabidopsis. , 1997, Development.

[22]  Martin A. Nowak,et al.  Evolution of genetic redundancy , 1997, Nature.

[23]  Wilson N. Stewart Paleobotany and the Evolution of Plants , 1983 .

[24]  Pea Compound Leaf Architecture Is Regulated by Interactions among the Genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS , 2000, Plant Cell.

[25]  M A Nowak,et al.  Evolutionary preservation of redundant duplicated genes. , 1999, Seminars in cell & developmental biology.

[26]  K. Shimamoto,et al.  Down-regulation of RFL, the FLO/LFY homolog of rice, accompanied with panicle branch initiation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  D. Dilcher Toward a new synthesis: major evolutionary trends in the angiosperm fossil record. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. Weigel,et al.  A genetic framework for floral patterning , 1998, Nature.

[29]  T. Nishiyama,et al.  Evolution of MADS-Box Gene Induction by FLO/LFY Genes , 2001, Journal of Molecular Evolution.

[30]  LEAFY and the evolution of rosette flowering in violet cress (Jonopsidium acaule, Brassicaceae). , 2000, American journal of botany.

[31]  Michael J. Donoghue,et al.  Seed plant phylogeny: Demise of the anthophyte hypothesis? , 2000, Current Biology.

[32]  Hong Ma,et al.  Missing links: the genetic architecture of flower and floral diversification , 2002 .

[33]  D. Weigel,et al.  NFL1, a Nicotiana tabacum LEAFY-like gene, controls meristem initiation and floral structure. , 2001, Plant & cell physiology.

[34]  D. Krakauer,et al.  Redundancy, antiredundancy, and the robustness of genomes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. Crepet Progress in understanding angiosperm history, success, and relationships: Darwin's abominably "perplexing phenomenon". , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[36]  C. dePamphilis,et al.  Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  W. Martin,et al.  Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support gnetalean affinities of angiosperms. , 1996, Molecular biology and evolution.

[38]  Y. Helariutta,et al.  Duplication and functional divergence in the chalcone synthase gene family of Asteraceae: evolution with substrate change and catalytic simplification. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[39]  A. Force,et al.  The probability of preservation of a newly arisen gene duplicate. , 2001, Genetics.

[40]  E. M. Gifford,et al.  Morphology and evolution of vascular plants , 1989 .

[41]  K. Nixon,et al.  Archaefructaceae, a New Basal Angiosperm Family , 2002, Science.

[42]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.