Flower development: open questions and future directions.

Almost three decades of genetic and molecular analyses have resulted in detailed insights into many of the processes that take place during flower development and in the identification of a large number of key regulatory genes that control these processes. Despite this impressive progress, many questions about how flower development is controlled in different angiosperm species remain unanswered. In this chapter, we discuss some of these open questions and the experimental strategies with which they could be addressed. Specifically, we focus on the areas of floral meristem development and patterning, floral organ specification and differentiation, as well as on the molecular mechanisms underlying the evolutionary changes that have led to the astounding variations in flower size and architecture among extant and extinct angiosperms.

[1]  Patrick Laufs,et al.  MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems , 2004, Development.

[2]  N. Kleckner,et al.  Meiotic chromosomes: integrating structure and function. , 1999, Annual review of genetics.

[3]  D. Ehrhardt,et al.  Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules , 2006, Science.

[4]  M. Kater,et al.  Uncovering genetic and molecular interactions among floral meristem identity genes in Arabidopsis thaliana. , 2012, The Plant journal : for cell and molecular biology.

[5]  M. Mandel,et al.  A gene triggering flower formation in Arabidopsis , 1995, Nature.

[6]  D. Smyth,et al.  PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana. , 2012, The Plant journal : for cell and molecular biology.

[7]  J. Bowman,et al.  The flowering hormone florigen functions as a general systemic regulator of growth and termination , 2009, Proceedings of the National Academy of Sciences.

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

[9]  E. Álvarez-Buylla,et al.  An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Elliot M. Meyerowitz,et al.  Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries , 1995, Nature.

[11]  Hong Ma,et al.  The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. , 2002, Genes & development.

[12]  G. Coupland,et al.  The genetic basis of flowering responses to seasonal cues , 2012, Nature Reviews Genetics.

[13]  D. Luo,et al.  Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function , 2004, Development.

[14]  Cindy Gustafson-Brown,et al.  Regulation of the arabidopsis floral homeotic gene APETALA1 , 1994, Cell.

[15]  Hong Ma,et al.  Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity , 1992, Cell.

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

[17]  K. Ng,et al.  A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. , 2009, Genes & development.

[18]  A. Müller,et al.  Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. , 1998, Science.

[19]  Lixi Jiang,et al.  TAPETUM DETERMINANT1 Is Required for Cell Specialization in the Arabidopsis Anther Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016618. , 2003, The Plant Cell Online.

[20]  Toshiro Ito,et al.  Floral stem cells: from dynamic balance towards termination. , 2010, Biochemical Society transactions.

[21]  G. Theißen,et al.  MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. , 1999, Developmental genetics.

[22]  S. Briggs,et al.  Diversification of C-Function Activity in Maize Flower Development , 1996, Science.

[23]  C. Ferrándiz,et al.  Gynoecium Patterning in Arabidopsis: A Basic Plan behind a Complex Structure , 2009 .

[24]  Shujing Liu,et al.  Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development , 2012, Proceedings of the National Academy of Sciences.

[25]  M. Hasebe,et al.  Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants , 1999, Evolution & development.

[26]  H. Dickinson,et al.  EXS, a Putative LRR Receptor Kinase, Regulates Male Germline Cell Number and Tapetal Identity and Promotes Seed Development in Arabidopsis , 2002, Current Biology.

[27]  E. Meyerowitz,et al.  Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. Wagner,et al.  A molecular framework for auxin-mediated initiation of flower primordia. , 2013, Developmental cell.

[29]  V. Walbot,et al.  Hypoxia Triggers Meiotic Fate Acquisition in Maize , 2012, Science.

[30]  J L Bowman,et al.  Genes directing flower development in Arabidopsis. , 1989, The Plant cell.

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

[32]  M. Lenhard,et al.  Termination of Stem Cell Maintenance in Arabidopsis Floral Meristems by Interactions between WUSCHEL and AGAMOUS , 2001, Cell.

[33]  P. Springer,et al.  Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries , 2012, Proceedings of the National Academy of Sciences.

[34]  Arezki Boudaoud,et al.  Mechanical Regulation of Auxin-Mediated Growth , 2012, Current Biology.

[35]  H Fujisawa,et al.  Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. , 1997, The Plant cell.

[36]  M. Svensson,et al.  Closely related MADS-box genes in club moss (Lycopodium) show broad expression patterns and are structurally similar to, but phylogenetically distinct from, typical seed plant MADS-box genes. , 2002, The New phytologist.

[37]  B. Causier,et al.  The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[38]  M. Grelon,et al.  Meiosis in plants: ten years of gene discovery , 2008, Cytogenetic and Genome Research.

[39]  Karen S. Osmont,et al.  Comprehensive Analysis of CLE Polypeptide Signaling Gene Expression and Overexpression Activity in Arabidopsis1[C][W][OA] , 2010, Plant Physiology.

[40]  Xiaochun Ge,et al.  Signaling and Transcriptional Control of Reproductive Development in Arabidopsis , 2010, Current Biology.

[41]  R. Amasino Seasonal and developmental timing of flowering. , 2010, The Plant journal : for cell and molecular biology.

[42]  E. Meyerowitz,et al.  The Homeotic Protein AGAMOUS Controls Late Stamen Development by Regulating a Jasmonate Biosynthetic Gene in Arabidopsis[W] , 2007, The Plant Cell Online.

[43]  G. Haughn,et al.  LEAFY, a Homeotic Gene That Regulates Inflorescence Development in Arabidopsis. , 1991, The Plant cell.

[44]  Hong Ma A Molecular Portrait of Arabidopsis Meiosis , 2006, The arabidopsis book.

[45]  I. Sussex,et al.  Function of the apetala-1 gene during Arabidopsis floral development. , 1990, The Plant cell.

[46]  C. Smaczniak,et al.  Target Genes of the MADS Transcription Factor SEPALLATA3: Integration of Developmental and Hormonal Pathways in the Arabidopsis Flower , 2009, PLoS biology.

[47]  Cindy Gustafson-Brown,et al.  Molecular characterization of the Arabidopsis floral homeotic gene APETALA1 , 1992, Nature.

[48]  M. Kater,et al.  AGL24, SHORT VEGETATIVE PHASE, and APETALA1 Redundantly Control AGAMOUS during Early Stages of Flower Development in Arabidopsis[W] , 2006, The Plant Cell Online.

[49]  R. Sablowski,et al.  Genes and functions controlled by floral organ identity genes. , 2010, Seminars in cell & developmental biology.

[50]  Elliot M Meyerowitz,et al.  Floral homeotic genes are targets of gibberellin signaling in flower development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D. Wagner,et al.  The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER , 2006, Development.

[52]  Gerco C. Angenent,et al.  Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis , 2005, Development.

[53]  Hans Sommer,et al.  Ternary complex formation between the MADS‐box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus , 1999, The EMBO journal.

[54]  J. Bowman,et al.  Early flower development in Arabidopsis. , 1990, The Plant cell.

[55]  Hong Ma,et al.  The BAM1/BAM2 Receptor-Like Kinases Are Important Regulators of Arabidopsis Early Anther Development[W] , 2006, The Plant Cell Online.

[56]  J. Bowman,et al.  CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. , 1999, Development.

[57]  Martin Kieffer,et al.  TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis , 2011, The Plant journal : for cell and molecular biology.

[58]  E. Meyerowitz,et al.  Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem , 2005, Current Biology.

[59]  K. Shimamoto,et al.  Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. , 2000, Plant & cell physiology.

[60]  Aalt D J van Dijk,et al.  Characterization of SOC1’s Central Role in Flowering by the Identification of Its Upstream and Downstream Regulators1[C][W] , 2012, Plant Physiology.

[61]  C. Kuhlemeier,et al.  Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs , 2000, Plant Cell.

[62]  T. Payne,et al.  KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium , 2004, Development.

[63]  J. Bowman,et al.  Genetic interactions among floral homeotic genes of Arabidopsis. , 1991, Development.

[64]  Hong Ma,et al.  Molecular control of microsporogenesis in Arabidopsis. , 2011, Current opinion in plant biology.

[65]  E. Coen,et al.  Separation of genetic functions controlling organ identity in flowers , 2003, The EMBO journal.

[66]  H. Sommer,et al.  Multiple interactions amongst floral homeotic MADS box proteins. , 1996, The EMBO journal.

[67]  Yingzhen Yang,et al.  DORNRÖSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis , 2007, Plant Molecular Biology.

[68]  M. Kater,et al.  AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[69]  P. Comelli,et al.  DORNRÖSCHEN-LIKE expression marks Arabidopsis floral organ founder cells and precedes auxin response maxima , 2011, Plant Molecular Biology.

[70]  Rainer Melzer,et al.  Reconstitution of ‘floral quartets’ in vitro involving class B and class E floral homeotic proteins , 2009, Nucleic acids research.

[71]  W. Nacken,et al.  Genetic Control of Flower Development by Homeotic Genes in Antirrhinum majus , 1990, Science.

[72]  Zhongchi Liu,et al.  APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development , 2006, Development.

[73]  G. Ditta,et al.  Assessing the redundancy of MADS-box genes during carpel and ovule development , 2003, Nature.

[74]  F. Wellmer,et al.  Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA , 2012, Proceedings of the National Academy of Sciences.

[75]  J. Nemhauser,et al.  Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. , 2000, Development.

[76]  M. Hasebe,et al.  Characterization of MADS homeotic genes in the fern Ceratopteris richardii. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Hong Ma,et al.  The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors , 1990, Nature.

[78]  P. Bhalla,et al.  Control of male germ‐cell development in flowering plants , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[79]  J. Bowman,et al.  Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product , 1991, Cell.

[80]  S. Masiero,et al.  Ternary Complex Formation between MADS-box Transcription Factors and the Histone Fold Protein NF-YB* , 2002, The Journal of Biological Chemistry.

[81]  Shane T. Jensen,et al.  LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. , 2011, Developmental cell.

[82]  Y. Couder,et al.  Developmental Patterning by Mechanical Signals in Arabidopsis , 2009 .

[83]  P. M. Sanders,et al.  Anther developmental defects in Arabidopsis thaliana male-sterile mutants , 1999, Sexual Plant Reproduction.

[84]  K. Tandre,et al.  Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. , 1998, The Plant journal : for cell and molecular biology.

[85]  W. Crosby,et al.  APETALA1 and SEPALLATA3 interact to promote flower development. , 2001, The Plant journal : for cell and molecular biology.

[86]  Hong Ma,et al.  The AtRAD51C Gene Is Required for Normal Meiotic Chromosome Synapsis and Double-Stranded Break Repair in Arabidopsis1 , 2005, Plant Physiology.

[87]  Huai Wang,et al.  A transcriptional repression motif in the MADS factor AGL15 is involved in recruitment of histone deacetylase complex components. , 2008, The Plant journal : for cell and molecular biology.

[88]  G. Theißen,et al.  Conserved differential expression of paralogous DEFICIENS- and GLOBOSA-like MADS-box genes in the flowers of Orchidaceae: refining the 'orchid code'. , 2011, The Plant journal : for cell and molecular biology.

[89]  B. Ambrose,et al.  Poppy APETALA1/FRUITFULL Orthologs Control Flowering Time, Branching, Perianth Identity, and Fruit Development1[W][OA] , 2012, Plant Physiology.

[90]  Hong Ma,et al.  The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. , 2005, Molecular biology of the cell.

[91]  Kerstin Kaufmann,et al.  Regulation of transcription in plants: mechanisms controlling developmental switches , 2010, Nature Reviews Genetics.

[92]  Elliot M. Meyerowitz,et al.  Cytokinin signaling as a positional cue for patterning the apical–basal axis of the growing Arabidopsis shoot meristem , 2012, Proceedings of the National Academy of Sciences.

[93]  D. Wagner,et al.  Genomic identification of direct target genes of LEAFY. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[94]  Heinz Saedler,et al.  Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes , 1996, Journal of Molecular Evolution.

[95]  E. Mjolsness,et al.  An auxin-driven polarized transport model for phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[96]  Elliot M. Meyerowitz,et al.  Orchestration of Floral Initiation by APETALA1 , 2010, Science.

[97]  J. Zethof,et al.  A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity , 2007, Nature Genetics.

[98]  B. Causier,et al.  An Antirrhinum ternary complex factor specifically interacts with C-function and SEPALLATA-like MADS-box factors , 2003, Plant Molecular Biology.

[99]  James M. Whitacre,et al.  Degeneracy: a link between evolvability, robustness and complexity in biological systems , 2009, Theoretical Biology and Medical Modelling.

[100]  Elliot M Meyerowitz,et al.  Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness , 2007, Development.

[101]  P. Ciceri,et al.  Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. , 2000, Molecular cell.

[102]  Xuemei Chen,et al.  Orchestration of the Floral Transition and Floral Development in Arabidopsis by the Bifunctional Transcription Factor APETALA2[W][OA] , 2010, Plant Cell.

[103]  I. Golubovskaya Genetic control of meiosis. , 1979, International review of cytology.

[104]  H. Philippe,et al.  Resolving Difficult Phylogenetic Questions: Why More Sequences Are Not Enough , 2011, PLoS biology.

[105]  Axel Bender,et al.  Degeneracy: a design principle for achieving robustness and evolvability. , 2009, Journal of theoretical biology.

[106]  J. Vrebalov,et al.  A MADS-Box Gene Necessary for Fruit Ripening at the Tomato Ripening-Inhibitor (Rin) Locus , 2002, Science.

[107]  O. Hamant,et al.  Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport , 2010, PLoS biology.

[108]  J. Long,et al.  Initiation of axillary and floral meristems in Arabidopsis. , 2000, Developmental biology.

[109]  E. Álvarez-Buylla,et al.  Conversion of leaves into petals in Arabidopsis , 2001, Current Biology.

[110]  E. Sanchez-Moran,et al.  Pathways to meiotic recombination in Arabidopsis thaliana. , 2011, The New phytologist.

[111]  A. Bleecker,et al.  Axillary meristem development in Arabidopsis thaliana. , 2000, The Plant journal : for cell and molecular biology.

[112]  D. Wagner,et al.  Transcriptional activation of APETALA1 by LEAFY. , 1999, Science.

[113]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[114]  E. Meyerowitz,et al.  Genome-Wide Analysis of Gene Expression during Early Arabidopsis Flower Development , 2006, PLoS genetics.

[115]  L. Feldman,et al.  Photoinduction of Flower Identity in Vegetatively Biased Primordia , 1998, Plant Cell.

[116]  G. Theißen,et al.  Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[117]  Hong Ma,et al.  Genetics of meiotic prophase I in plants. , 2006, Annual review of plant biology.

[118]  E. Coen,et al.  Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. , 1990, Genes & development.

[119]  Hong Ma Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. , 2005, Annual review of plant biology.

[120]  L. Vázquez-Moreno,et al.  Floral transcription factor AGAMOUS interacts in vitro with a leucine-rich repeat and an acid phosphatase protein complex. , 2001, Biochemical and biophysical research communications.

[121]  D. Weigel,et al.  SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. , 1992, Development.

[122]  P. M. Santiago,et al.  Elaboration of B Gene Function to Include the Identity of Novel Floral Organs in the Lower Eudicot Aquilegia[W] , 2007, The Plant Cell Online.

[123]  B. Rannala,et al.  Molecular phylogenetics: principles and practice , 2012, Nature Reviews Genetics.

[124]  M. Bennett,et al.  Regulation of phyllotaxis by polar auxin transport , 2003, Nature.

[125]  A. Litt An Evaluation of A‐Function: Evidence from the APETALA1 and APETALA2 Gene Lineages , 2007, International Journal of Plant Sciences.

[126]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[127]  Hong Ma,et al.  The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[128]  L. Feldman,et al.  Bi-directional inflorescence development inArabidopsis thaliana: Acropetal initiation of flowers and basipetal initiation of paraclades , 2004, Planta.

[129]  M. Schmid,et al.  Regulation of flowering time: all roads lead to Rome , 2011, Cellular and Molecular Life Sciences.

[130]  H. Saedler,et al.  Evolutionary aspects of MADS-box genes in the eusporangiate fern Ophioglossum , 2002 .

[131]  Elliot M. Meyerowitz,et al.  Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes , 1993 .

[132]  J. Bowman,et al.  Turning floral organs into leaves, leaves into floral organs. , 2001, Current opinion in genetics & development.

[133]  Jianping Lu,et al.  CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum , 2004, Development.

[134]  G. Edelman,et al.  Degeneracy and complexity in biological systems , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[135]  M. Yanofsky,et al.  Molecular basis of the cauliflower phenotype in Arabidopsis , 1995, Science.

[136]  C. Helliwell,et al.  FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[137]  G. Theißen,et al.  A DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. , 1999, Developmental genetics.

[138]  E. Coen,et al.  Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of antirrhinum , 1993, Cell.

[139]  R. Martienssen,et al.  Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. , 2000, Development.

[140]  J. Beltrán,et al.  Isolation of mtpim Proves Tnt1 a Useful Reverse Genetics Tool in Medicago truncatula and Uncovers New Aspects of AP1-Like Functions in Legumes1 , 2006, Plant Physiology.

[141]  R. Simon,et al.  Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. , 1999, Science.

[142]  Lisha Shen,et al.  Regulation of floral patterning by flowering time genes. , 2009, Developmental cell.