Floral initiation and inflorescence architecture: A comparative view

Annals of Botany

Volumn 100, Issue 3, 2007, Pages 659-676

  Benlloch, Reyes ^a,b   Berbel, Ana ^a   Serrano Mislata, Antonio ^a   Madueño, Francisco ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

^b CEA GRENOBLE   (France)

Author keywords

APETALA1; Compound inflorescence; DET; Floral meristem identity; Inflorescence development; LEAFY; Legume; Plant architecture; TERMINAL FLOWER1; VEG1

Indexed keywords

COMPARATIVE STUDY; DICOTYLEDON; FLOWERING; GENE EXPRESSION; LEGUME; MORPHOLOGY;

FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; PLANT; REVIEW;

FLOWERS; GENE EXPRESSION REGULATION, PLANT; PLANTS;

ANTIRRHINUM; ANTIRRHINUM MAJUS; ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 34548237442     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcm146     Document Type: Review

References (113)

1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, et al. 2005. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056.
2. Ahearn KP, Johnson HA, Weigel D, Wagner DR. 2001. NFL1, a Nicotiana tabacum LEAFY-like gene, controls meristem initiation and floral structure. Plant Cell Physiology 42: 1130-1139.
3. Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, et al. 2006. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO Journal 25: 605-614.
4. Alvarez J, Guli CL, Yu X-H, Smyth DR. 1992. TERMINAL FLOWER: a gene affecting inflorescence development in Arabidopsis thaliana. Plant Journal 2: 103-116.
5. Amaya I, Ratcliffe OJ, Bradley DJ. 1999. Expression of CENTRORADIALIS (CEN) and CEN-like genes in tobacco reveals a conserved mechanism controlling phase change in diverse species. The Plant Cell 11: 1405-1418.
6. Baum DA, Yoon H-S, Oldham RL. 2005. Molecular evolution of the transcription factor LEAFY in Brassicaceae. Molecular Phylogenetics and Evolution 37: 1-14.
7. Benlloch R, d'Erfurth I, Ferrándiz C, Cosson V, Beltrán JP, Canas LA, et al. 2006. Isolation of mtpim proves Tnt1 a useful reverse genetics tool in Medicago truncatula and uncovers new aspects of AP1-like functions in legumes. Plant Physiology 142: 972-983.
8. Berbel A, Navarro C, Ferrándiz C, Canas LA, Madueño F, Beltrán JP. 2001. Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. Plant Journal 25: 441-451.
9. Blázquez MA, Weigel D. 2000. Integration of floral inductive signals in Arabidopsis. Nature 404: 889-892.
10. Blázquez MA, Soowal LN, Lee I, Weigel D. 1997. LEAFY expression and flower initiation in Arabidopsis. Development 124: 3835-3844.
11. Blázquez MA, Ferrándiz C, Madueño F, Parcy F. 2006. How floral meristems are built. Plant Molecular Biology 60: 855-870.
12. Bommert P, Satoh-Nagasawa N, Jackson D, Hirano H-Y. 2005. Genetics and evolution of inflorescence and flower development in Grasses. Plant Cell Physiology 46: 69-78.
13. Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR. 1993. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119: 721-743.
14. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E. 1996. Control of inflorescence architecture in Antirrhinum. Nature 379: 791-797.
15. Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E. 1997. Inflorescence commitment and architecture in Arabidopsis. Science 275: 80-83.
16. Calonje M, Cubas P, Martínez-Zapater JM, Carmona MJ. 2004. Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiology 135: 1491-1501.
17. Carmel-Goren L, Liu YS, Lifschitz E, Zamir D. 2003. The SELFPRUNING gene family in tomato. Plant Molecular Biology 52: 1215-1222.
18. Carmona MJ, Cubas P, Martínez-Zapater JM. 2002. VFL, the grapevine FLORICAULA/LEAFY ortholog, is expressed in meristematic regions independently of their fate. Plant Physiology 130: 68-77.
19. Carmona MJ, Calonje M, Martínez-Zapater JM. 2007. The FT/TFL1 gene family in grapevine. Plant Molecular Biology 63: 637-650.
20. Chardon F, Damerval C. 2005. Phylogenomic analysis of the PEBP gene family in cereals. Journal of Molecular Evolution 61: 579-590.
21. Chautard H, Jacquet M, Schoentgen F, Bureaud N, Benedetti H. 2004. Tfs1p, a member of the PEBP family, inhibits the Ira2p but not the Ira1p Ras GTPase-activating protein in Saccharomyces cerevisiae. Eukaryotic Cell 3: 459-470.
22. Coen ES, Nugent JM. 1994. Evolution of flowers and inflorescences. Development Supplement: 107-116.
23. Coen ES, Romero JM, Doyle S, Elliott R, Murphy G, Carpenter R. 1990. Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63: 1311-1322.
24. Cremer F, Lonnig WE, Saedler H, Huijser P. 2001. The delayed terminal flower phenotype is caused by a conditional mutation in the CENTRORADIALIS gene of snapdragon. Plant Physiology 126: 1031-1041.
25. Doebley J, Lukens L. 1998. Transcriptional regulators and the evolution of plant form. The Plant Cell 10: 1075-1082.
26. Domoney C, Duc G, Ellis THN, Ferrándiz C, Firnhaber C, Gallardo K, et al. 2006. Genetic and genomic analysis of legume flowers and seeds. Current Opinion in Plant Biology 9: 133-141.
27. Dong ZC, Zhao Z, Liu CW, Luo JH, Yang J, Huang WH, et al. 2005. Floral patterning in Lotus japonicus. Plant Physiology 137: 1272-1282.
28. Dornelas MC, Rodríguez APM. 2005. The rubber tree (Hevea brasiliensis Muell. Arg.) homologue of the LEAFY/FLORICAULA gene is preferentially expressed in both male and female floral meristems. Journal of Experimental Botany 56: 1965-1974.
29. Elo A, Lemmetyinen J, Turunen M-L, Tikka L, Sopanen T. 2001. Three MADS-box genes similar to APETALA 1 and FRUITFULL from silver birch (Betula pendula). Physiologia Plantarum 112: 95-103.
30. Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF. 2000. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127: 725-734.
31. Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, Banfield MJ, Rameau C. 2003. DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. The Plant Cell 15: 2742-2754.
32. Frolich MW, Parker DS. 2000. The mostly male theory of flower evolutionary origins: from genes to fossils. Systematic Botany 25: 155-170.
33. Gu Q, Ferrándiz C, Yanofsky MF, Martienssen R. 1998. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509-1517.
34. Guo X, Zhao Z, Chena J, Hua X, Luo D. 2006. A putative CENTRORADIALIS/TERMINAL FLOWER1-like gene, Ljcen1, plays a role in phase transition in Lotus japonicus. Journal of Plant Physiology 163: 436-444.
35. Hanzawa Y, Money T, Bradley D. 2005. A single amino acid converts a repressor to an activator of flowering. Proceedings of the National Academy of Sciences of the USA 102: 7748-7753.
36. Hardenack S, Ye D, Saedler H, Grant S. 1994. Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion. The Plant Cell 6: 1775-1787.
37. Hecht V, Foucher F, Ferrándiz C, Macknight R, Navarro C, Morin J, et al. 2005. Conservation of Arabidopsis flowering genes in model legumes. Plant Physiology 137: 1420-1434.
38. Hempel FD, Weigel D, Mandel MA, Ditta G, Zambryski PC, Feldman LJ, Yanofsky MF. 1997. Floral determination and expression of floral regulatory genes in Arabidopsis. Development 124: 3845-3853.
39. Hengst U, Albrecht H, Hess D, Monard D. 2001. The phosphatidylethanolamine-binding protein is the prototype of a novel family of serine protease inhibitors. Journal of Biological Chemistry 276: 535-540.
40. Hofer J, Ellis N. 2002. Conservation and diversification of gene function in plant development. Current Opinion in Plant Biology 5: 56-61.
41. Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N. 1997. UNIFOLIATA regulates leaf and flower morphogenesis in pea. Current Biology 7: 581-587.
42. Huala E, Sussex IM. 1992. LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development. Plant Cell 4: 901-903.
43. Huijser P, Klein J, Lonnig WE, Meijer H, Saedler H, Sommer H. 1992. Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO Journal 11: 1239-1249.
44. Ingram GC, Goodrich J, Wilkinson MD, Simon R, Haughn GW, Coen ES. 1995. Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. The Plant Cell 7: 1501-1510.
45. Irish VF, Sussex IM. 1990. Function of the apetala-1 gene during Arabidopsis floral development. The Plant Cell 2: 741-753.
46. Jack T. 2004. Molecular and genetic mechanisms of floral control. The Plant Cell 16: S1-S17.
47. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, et al. 1999. Activation tagging of the floral inducer FT. Science 286: 1962-1965.
48. Kellogg EA. 2007. Floral displays: genetic control of grass inflorescences. Current Opinion in Plant Biology 10: 26-31.
49. Kelly AJ, Bonnlander MB, Meeks-Wagner DR. 1995. NFL, the tobacco homolog of FLORICAULA and LEAFY, is transcriptionally expressed in both vegetative and floral meristems. The Plant Cell 7: 225-234.
50. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. 1999. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286: 1960-1962.
51. Kotoda N, Wada M. 2005. MdTFL1, a TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic Arabidopsis. Plant Science 168: 95-104.
52. Kotoda N, Wada M, Masuda T, Soejima J. 2003. The break-through in the reduction of juvenile phase in apple using transgenic approaches. Acta Horticulturae (ISHS) 625: 337-343.
53. Lawton-Rauh AL, Buckler IV ES, Purugganan MD. 1999. Patterns of molecular evolution among paralogous floral homeotic genes. Molecular Biology and Evolution 16: 1037-1045.
54. Leebens-Mack J, Soltis DE, Soltis PS. 2005. Plant reproductive genomics at the plant and animal genome conference. Comparative and functional genomics 6: 159-169.
55. Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS, Yanofsky MF. 1999. Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. The Plant Cell 11: 1007-1018.
56. Litt A, Irish VF. 2003. Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165: 821-833.
57. Lowman AC, Purugganan MD. 1999. Duplication of the Brassica oleracea APETALA1 floral homeotic gene and the evolution of domesticated cauliflower. The American Genetic Association 90: 514-520.
58. Maizel A, Busch MA, Tanahashi T, Perkovic J, Kato M, Hasebe M, Weigel D. 2005. The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308: 260-263.
59. Mandel AM, Yanofsky MF. 1995. A gene triggering flower formation in Arabidopsis. Nature 377: 522-524.
60. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF. 1992. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273-277.
61. Mellerowicz EJ, Horgan K, Walden A, Coker A, Walter C. 1998. PRFLL, a Pinus radiata homologue of FLORICAULA and LEAFY is expressed in buds containing vegetative shoot and undifferentiated male cone primordia. Planta 206: 619-629.
62. Mimida N, Goto K, Kobayashi Y, Araki T, Ahn JH, Weigel D, et al. 2001. Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes to Cells 6: 327-336.
63. Molinero-Rosales N, Jamilena M, Zurita S, Gomez P, Capel J, Lozano R. 1999. FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant Journal 20: 685-693.
64. Mouradov A, Glassick T, Hamdorf B, Murphy L, Fowler B, Marla S, Teasdale RD. 1998. NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems. Proceedings of the National Academy of Sciences of the USA 95: 6537-6542.
65. Murfet IC. 1992. Garden pea and allies - an update from Hobart. Flowering Newsletter 13: 10-20.
66. Ohshima S, Murata M, Sakamoto W, Ogura Y, Motoyoshi F. 1997. Cloning and molecular analysis of the Arabidopsis gene TERMINAL FLOWER 1. Molecular General Genetics 254: 186-194.
67. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD. 1997. The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 94: 7076-7081.
68. Ordidge M, Chiurugwi T, Tooke F, Battey NH. 2005. LEAFY, TERMINAL FLOWER1 and AGAMOUS are functionally conserved but do not regulate terminal flowering and floral determinacy in Impatiens balsamina. Plant Journal 44: 985-1000.
69. Parcy F. 2005. Flowering: a time for integration. The International Journal of Developmental Biology 49: 585-593.
70. Parcy F, Nilsson O, Busch MA, Lee I, Weigel D. 1998. A genetic framework for floral patterning. Nature 395: 561-566.
71. Parcy F, Bomblies K, Weigel D. 2002. Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral meristem identity in Arabidopsis. Development 129: 2519-2527.
72. Parkin J. 1914. The evolution of the inflorescence. Linnean Journal of Botany 42: 511-562.
73. Pillitteri LJ, Lovatt CJ, Walling LL. 2004. Isolation and characterization of a TERMINAL FLOWER homolog and its correlation with juvenility in citrus. Plant Physiology 135: 1540-1551.
74. Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Álvarez J, Ganal M, Zamir D, Lifschitz E. 1998. The SELFPRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125: 1979-1989.
75. Pouteau S, Nicholls D, Tooke F, Coen E, Battey N. 1997. The induction and maintenance of flowering in Impatiens. Development 124: 3343-3351.
76. Pouteau S, Tooke F, Battey N. 1998. Quantitative control of inflorescence formation in Impatiens balsamina. Plant Physiology 118: 1191-1201.
77. Prusinkiewicz P, Erasmus Y, Lane B, Harder LD, Coen E. 2007. Evolution and development of inflorescence architectures. Science 136: 1452-1456.
78. Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ. 1998. A common mechanism controls the life cycle and architecture of plants. Development 125: 1609-1615.
79. Ratcliffe OJ, Bradley DJ, Coen ES. 1999. Separation of shoot and floral identity in Arabidopsis. Development 126: 1109-1120.
80. Reid JB, Murfet IC. 1984. Flowering in Pisum: a fifth locus, Veg. Annals of Botany 53: 369-382.
81. Reid JB, Murfet IC, Singer SR, Weller JL, Taylor SA. 1996. Physiological-genetics of flowering in Pisum. Cell and Developmental Biology 7: 455-463.
82. Rottmann WH, Meilan R, Sheppard LA, Brunner AM, Skinner JS, Ma C, et al. 2000. Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant Journal 22: 235-245.
83. Savidge B. 1996. Floral meristem specification and floral organ development in Arabidopsis. PhD dissertation, University of California at San Diego, La Jolla, California, La Jolla, USA.
84. Schultz EA, Haughn GW. 1991. LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3: 771-781.
85. Schultz EA, Haughn GW. 1993. Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development 119: 745-765.
86. Shannon S, Meeks-Wagner DR. 1991. A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. The Plant Cell 3: 877-892.
87. Shu G, Amaral W, Hileman LC, Baum DA. 2000. Leafy and the evolution of rosette flowering in violet cress (Jonopsidium acaule, Brassicaceae). American Journal of Botany 87: 634-641.
88. Singer SR, Hsuing LP, Huber SC. 1990. Determinate (det) mutant of Pisum sativum L. (Leguminosae: Papilionoideae) exhibits an indeterminate growth pattern. American Journal of Botany 77: 1330-1335.
89. Singer SR, Maki SL, Mullen HJ. 1994. Specification of meristem identity in Pisum sativum inflorescence development. Flowering Newsletter 18: 26-32.
90. Singer S, Sollinger J, Maki S, Fishbach J, Short B, Reinke C, Fick J, Cox L. 1999. Inflorescence architecture: a developmental genetics approach. The Botanical review 65: 385-410.
91. Sliwinski MK, White MA, Maizel A, Weigel D, Baum DA. 2006. Evolutionary divergence of LFY function in the mustards Arabidopsis thaliana and Leavenworthia crassa. Plant Molecular Biology 62: 279-289.
92. Soltis DE, Soltis PS. 2003. The role of phylogenetics in comparative genetics. Plant Physiology 132: 1790-1800.
93. Souer E, van der Krol A, Kloos D, Spelt C, Bliek M, Mol J, Koes R. 1998. Genetic control of branching pattern and floral identity during Petunia inflorescence development. Development 125: 733-742.
94. Southerton SG, Strauss SH, Olive MR, Harcourt RL, Decroocq V Zhu X, et al. 1998. Eucalyptus has a functional equivalent of the Arabidopsis floral meristem identity gene LEAFY. Plant Molecular Biology 37: 897-910.
95. Sreekantan L, Clemens J, McKenzie MJ, Lenton JR, Croker SJ, Jameson PE. 2004. Flowering genes in Metrosideros fit a broad herbaceous model encompassing Arabidopsis and Antirrhinum. Physiologia Plantarum 121: 163-173.
96. Stebbins GL. 1974. Flowering plants: evolution above the species sevel. Cambridge, MA: Harvard University Press.
97. Tanahashi T, Sumikawa N, Kato M, Hasebe M. 2005. Diversification of gene function: homologs of the floral regulator FLO/LFY control the first zygotic cell division in the moss Physcomitrella patens. Development 132: 1727-1736.
98. Taylor SA, Hofer JM, Murfet IC, Sollinger JD, Singer SR, Knox MR, Ellis TH. 2002. PROLIFERATING INFLORESCENCE MERISTEM, a MADS-box gene that regulates floral meristem identity in pea. Plant Physiology 129: 1150-1159.
99. Tucker SC, Grimes J. 1999. The inflorescence: introduction. The Botanical Review 65: 303-316.
100. Vijayraghavan U, Prasad K, Meyerowitz E. 2005. Specification and maintenance of the floral meristem: interactions between positively acting promoters of flowering and negative regulators. Current Science 89: 1835-1843.
101. Wada M, Cao QF, Kotoda N, Soejima J, Masuda T. 2002. Apple has two orthologues of FLORICAULA/LEAFY involved in flowering. Plant Molecular Biology 49: 567-577.
102. Wagner D, Sablowski RWM, Eyerowitz EM. 1999. Transcriptional activation of APETALA1 by LEAFY. Science 285: 582-584.
103. Walton EF, Podivinsky E, Wu RM. 2001. Bimodal patterns of floral gene expression over the two seasons that kiwifruit flowers develop. Physiologia Plantarum 111: 396-404.
104. Weberling F. 1989a. Morphology of flowers and inflorescences, 1st edn. Cambridge, UK: Cambridge University Press.
105. Weberling F. 1989b. Structure and evolutionary tendencies of inflorescences in the Leguminosae. In: Stirton CH, Zarucchi JL, eds. Advances in legume biology. Monographs in Systematic Botany. Missouri: Missouri Botanical Garden, 29: 35-58.
106. Weigel D, Nilsson O. 1995. A developmental switch sufficient for flower initiation in diverse plants. Nature 377: 495-500.
107. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM. 1992. LEAFY controls floral meristem identity in Arabidopsis. Cell 69: 843-859.
108. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059.
109. Wyatt R. 1982. Inflorescence architecture: how flower number, arrangement, and phenology affect pollination and fruit-set. American Journal of Botany 69: 585-594.
110. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, et al 1999. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401: 173-177.
111. Yoon H-S, Baum DA. 2004. Transgenic study of parallelism in plant morphological evolution. Proceedings of the National Academy of Sciences of the USA 101: 6524-6529.
112. Yu D, Kotilainen M, Pollanen E, Mehto M, Elomaa P, Helariutta Y, Albert VA, Teeri TH. 1999. Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant Journal 17: 51-62.
113. Yu H, Xu Y, Tan EL, Kumar PP. 2002. AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proceedings of the National Academy of Sciences of the USA 99: 16336-16341.