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The ABC of Flower Development in Monocots: The Model of Rice Spikelet

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Flower Development

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2686))

Abstract

The initial seminal studies of flower developmental genetics were made from observations in several eudicot model species, particularly Arabidopsis and Antirrhinum. However, an increasing amount of research in monocot model and crop species is finally giving the credit that monocots deserve for their position in the evolutionary history of Angiosperms, their astonishing diversification and adaptation, their diversified floral structures, their pivotal function in most ecosystems on Earth and, finally, their importance in agriculture and farming, economy, landscaping and feeding mankind. Rice is a staple crop and the major monocot model to study the reproductive phase and flower evolution. Inspired by this, this chapter reviews a story of highly conserved functions related to the ABC model of flower development. Nevertheless, this model is complicated in rice by cases of gene neofunctionalization, like the recruitment of MADS-box genes for the development of the unique organs known as lemma and palea, subfunctionalization, and rewiring of conserved molecular pathways.

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References

  1. Stevens PF (2001 onwards) Angiosperm phylogeny website. Version 14 July 2017 [and more or less continuously updated since]. http://www.mobot.org/MOBOT/research/APweb/

  2. Buzgo M, Endress PK (2000) Floral structure and development of acoraceae and its systematic relationships with basal angiosperms. Int J Plant Sci 161:23–41

    Article  CAS  PubMed  Google Scholar 

  3. Rudall PJ, Bateman RM (2004) Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytol 162:25–44. https://doi.org/10.1111/J.1469-8137.2004.01032.X

    Article  Google Scholar 

  4. Vergara-Silva F, Espinosa-Matías S, Ambrose BA, Vázquez-Santana S, Martínez-Mena A, Márquez-Guzmán J, Martínez E, Meyerowitz EM, Alvarez-Buylla ER (2003) Inside-out flowers characteristic of Lacandonia schismatica evolved at least before its divergence from a closely related taxon, Triuris brevistylis. Int J Plant Sci 164:345–357. https://doi.org/10.1086/368235

    Article  Google Scholar 

  5. Álvarez-Buylla ER, Ambrose BA, Flores-Sandoval E, Vergara-Silva F, Englund M, Garay-Arroyo A, García-Ponce B, de la Torre-Bárcena E, Espinosa-Matías S, Martínez E et al (2010) B-function expression in the flower center underlies the homeotic phenotype of Lacandonia schismatica (Triuridaceae). Plant Cell 22:3543–3559. https://doi.org/10.1105/tpc.109.069153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Aliscioni S, Bell HL, Besnard G, Christin PA, Columbus JT, Duvall MR, Edwards EJ, Giussani L, Hasenstab-Lehman K, Hilu KW et al (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312. https://doi.org/10.1111/J.1469-8137.2011.03972.X

    Article  CAS  Google Scholar 

  7. Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes RR, Zhang F et al (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated Rice. Nature 557:43–49. https://doi.org/10.1038/s41586-018-0063-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Gordon SP, Contreras-Moreira B, Woods DP, Des Marais DL, Burgess D, Shu S, Stritt C, Roulin AC, Schackwitz W, Tyler L (2017) Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nat Commun 8:2184. https://doi.org/10.1038/s41467-017-02292-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chapman MA, He Y, Zhou M (2022) Beyond a reference genome: pangenomes and population genomics of underutilized and orphan crops for future food and nutrition security. New Phytol 234:1583–1597

    Article  PubMed  PubMed Central  Google Scholar 

  10. Gui S, Wei W, Jiang C, Luo J, Chen L, Wu S, Li W, Wang Y, Li S, Yang N et al (2022) A pan-Zea genome map for enhancing maize improvement. Genome Biol 23:178. https://doi.org/10.1186/s13059-022-02742-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hufford MB, Seetharam AS, Woodhouse MR, Chougule KM, Ou S, Liu J, Ricci WA, Guo T, Olson A, Qiu Y et al (2021) De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science 373:655–662. https://doi.org/10.1126/science.abg5289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, Brinton J, Ramirez-Gonzalez RH, Kolodziej MC, Delorean E, Thambugala D et al (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature 588:277–283. https://doi.org/10.1038/s41586-020-2961-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100. https://doi.org/10.1126/science.1068275

    Article  CAS  PubMed  Google Scholar 

  14. Yu J, Hu S, Wang J, Wong GKS, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92. https://doi.org/10.1126/science.1068037

    Article  CAS  PubMed  Google Scholar 

  15. Kaul S, Koo HL, Jenkins J, Rizzo M, Rooney T, Tallon LJ, Feldblyum T, Nierman W, Benito MI, Lin X et al (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815. https://doi.org/10.1038/35048692

    Article  CAS  Google Scholar 

  16. Bommert P, Whipple C (2018) Grass inflorescence architecture and meristem determinacy. Semin Cell Dev Biol 79:37–47

    Article  PubMed  Google Scholar 

  17. Zhang D, Yuan Z (2014) Molecular control of grass inflorescence development. Annu Rev Plant Biol 65:553–578. https://doi.org/10.1146/annurev-arplant-050213-040104

    Article  CAS  PubMed  Google Scholar 

  18. Kellogg EA (2022) Genetic control of branching patterns in grass inflorescences. Plant Cell 34:3518–2533. https://doi.org/10.1093/plcell/koac080

    Article  Google Scholar 

  19. Soreng RJ, Davis JI (1998) Phylogenetics and character evolution in the grass family (Poaceae): simultaneous analysis of morphological and chloroplast DNA restriction site character sets. Bot Rev 64:1–85. https://doi.org/10.1007/BF02868851

    Article  Google Scholar 

  20. Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205. https://doi.org/10.1104/pp.125.3.1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Graça Sajo M, Pabón-Mora N, Jardim J, Stevenson DW, Rudall PJ (2012) Homologies of the flower and inflorescence in the early-divergent grass Anomochloa (Poaceae). Am J Bot 99:614–628. https://doi.org/10.3732/ajb.1100290

    Article  PubMed  Google Scholar 

  22. Sajo MG, Longhi-Wagner HM, Rudall PJ (2008) Reproductive morphology of the early-divergent grass Streptochaeta and its bearing on the homologies of the grass spikelet. Plant Syst Evol 275:245–255. https://doi.org/10.1007/s00606-008-0080-5

    Article  Google Scholar 

  23. Preston JC, Christensen A, Malcomber ST, Kellogg EA (2009) MADS-box gene expression and implications for developmental origins of the grass spikelet. Am J Bot 96:1419–1429. https://doi.org/10.3732/ajb.0900062

    Article  CAS  PubMed  Google Scholar 

  24. Dreni L, Osnato M, Kater MM (2013) The ins and outs of the rice AGAMOUS subfamily. Mol Plant 6:650–664. https://doi.org/10.1093/mp/sst019

    Article  CAS  PubMed  Google Scholar 

  25. Rudall PJ, Stuppy W, Cunniff J, Kellogg EA, Briggs BG (2005) Evolution of reproductive structures in grasses (Poaceae) inferred by sister-group comparison with their putative closest living relatives, Ecdeiocoleaceae. Am J Bot 92:1432–1443. https://doi.org/10.3732/ajb.92.9.1432

    Article  PubMed  Google Scholar 

  26. Kellogg EA (2015) Flowering plants. Monocots: Poaceae. In: Kubitzki K (ed) Vol XIII of: The families and genera of vascular plants. Springer, New York. ISBN 9783319153322

    Google Scholar 

  27. Grass Phylogeny Working Group, Barker NP, Clark LG, Davis JI, Duvall MR, Guala GF, Hsiao C, Kellogg EA, Linder HP (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373. https://doi.org/10.2307/3298585

    Article  Google Scholar 

  28. Kellogg EA (2009) The evolutionary history of Ehrhartoideae, Oryzeae, and Oryza. Rice 2:1–14

    Article  Google Scholar 

  29. Kobayashi K, Maekawa M, Miyao A, Hirochika H, Kyozuka J (2010) PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Plant Cell Physiol 51:47–57. https://doi.org/10.1093/pcp/pcp166

    Article  CAS  PubMed  Google Scholar 

  30. Gao X, Liang W, Yin C, Ji S, Wang H, Su X, Guo C, Kong H, Xue H, Zhang D (2019) The SEPALLATA-like gene OsMADS34 is required for Rice inflorescence and spikelet development. Plant Physiol 153:728–740. https://doi.org/10.1104/pp.110.156711

    Article  CAS  Google Scholar 

  31. Lin X, Wu F, Du X, Shi X, Liu Y, Liu S, Hu Y, Theißen G, Meng Z (2014) The pleiotropic SEPALLATA-like gene OsMADS34 reveals that the “empty glumes” of rice (Oryza sativa) spikelets are in fact rudimentary lemmas. New Phytol 202:689–702. https://doi.org/10.1111/nph.12657

    Article  CAS  PubMed  Google Scholar 

  32. Yoshida A, Suzaki T, Tanaka W, Hirano HY (2009) The homeotic gene long sterile Lemma (G1) specifies sterile lemma identity in the rice spikelet. Proc Natl Acad Sci USA 106:20103–22108. https://doi.org/10.1073/pnas.0907896106

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hong L, Qian Q, Zhu K, Tang D, Huang Z, Gao L, Li M, Gu M, Cheng Z (2010) ELE restrains empty glumes from developing into lemmas. J Genet Genomics 37:101–115. https://doi.org/10.1016/S1673-8527(09)60029-1

    Article  CAS  PubMed  Google Scholar 

  34. Li H, Xue D, Gao Z, Yan M, Xu W, Xing Z, Huang D, Qian Q, Xue Y (2009) A putative lipase gene EXTRA GLUME1 regulates both empty-glume fate and spikelet development in rice. Plant J 57:593–605. https://doi.org/10.1111/j.1365-313X.2008.03710.x

    Article  CAS  PubMed  Google Scholar 

  35. Zhuang H, Wang HL, Zhang T, Zeng XQ, Chen H, Wang ZW, Zhang J, Zheng H, Tang J, Ling YH et al (2020) NONSTOP GLumes1 encodes a C2H2 zinc finger protein that regulates spikelet development in rice. Plant Cell 32:392–413. https://doi.org/10.1105/tpc.19.00682

    Article  CAS  PubMed  Google Scholar 

  36. Yoshida A, Ohmori Y, Kitano H, Taguchi-Shiobara F, Hirano HY (2012) ABERRANT SPIKELET and PANICLE1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice. Plant J 70:327–339. https://doi.org/10.1111/j.1365-313X.2011.04872.x

    Article  CAS  PubMed  Google Scholar 

  37. Zhang T, Li Y, Ma L, Sang X, Ling Y, Wang Y, Yu P, Zhuang H, Huang J, Wang N et al (2017) LATERAL FLORET 1 induced the three-florets spikelet in rice. Proc Natl Acad Sci U S A 114:9984–9989. https://doi.org/10.1073/pnas.1700504114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Matsuoka M, Ichikawa H, Saito A, Tada Y, Fujimura T, Kano-Murakami Y (1993) Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell 5:1039–1048. https://doi.org/10.2307/3869625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Shi B, Zhang C, Tian C, Wang J, Wang Q, Xu T, Xu Y, Ohno C, Sablowsk R, Heisler MG et al (2016) Two-step regulation of a meristematic cell population acting in shoot branching in Arabidopsis. PLoS Genet 12:e1006168. https://doi.org/10.1371/journal.pgen.1006168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ren D, Li Y, He G, Qian Q (2019) Multifloret spikelet improves rice yield. New Phytol 225:2301–2306. https://doi.org/10.1111/nph.16303

    Article  PubMed  Google Scholar 

  41. Prasad K, Parameswaran S, Vijayraghavan U (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J 43:915–928. https://doi.org/10.1111/j.1365-313X.2005.02504.x

    Article  CAS  PubMed  Google Scholar 

  42. Lopez-Dee ZP, Wittich P, Pè ME, Rigola D, Del Buono I, Sari Gorla M, Kater MM, Colombo L (1999) OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet 25:237–244. https://doi.org/10.1002/(SICI)1520-6408(1999)25:3<237::AID-DVG6>3.0.CO;2-L

    Article  CAS  PubMed  Google Scholar 

  43. Itoh J-I, Nonomura K-I, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47. https://doi.org/10.1093/pcp/pci501

    Article  CAS  PubMed  Google Scholar 

  44. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579. https://doi.org/10.1016/S1097-2765(00)80450-5

    Article  CAS  PubMed  Google Scholar 

  45. Schrager-Lavelle A, Klein H, Fisher A, Bartlett M (2017) Grass flowers: an untapped resource for floral Evo-devo. J Syst Evol 55:525–541

    Article  Google Scholar 

  46. Lombardo F, Yoshida H (2015) Interpreting lemma and palea homologies: a point of view from rice floral mutants. Front Plant Sci 6:61. https://doi.org/10.3389/fpls.2015.00061

    Article  PubMed  PubMed Central  Google Scholar 

  47. Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochika H, Uchida E, Nagato Y, Yoshida H (2009) MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell 21:3008–3025. https://doi.org/10.1105/tpc.109.068742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Reinheimer R, Kellogg EA (2009) Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression is ancient and palea expression is new. Plant Cell 21:2591–2605. https://doi.org/10.1105/tpc.109.068239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Pautler M, Tanaka W, Hirano HY, Jackson D (2013) Grass meristems I: shoot apical meristem maintenance, axillary meristem determinacy and the floral transition. Plant Cell Physiol 54:302–312

    Article  CAS  PubMed  Google Scholar 

  50. Tanaka W, Pautler M, Jackson D, Hirano HY (2013) Grass meristems II: inflorescence architecture, flower development and meristem fate. Plant Cell Physiol 54:313–324

    Article  CAS  PubMed  Google Scholar 

  51. Zong J, Wang L, Zhu L, Bian L, Zhang B, Chen X, Huang G, Zhang X, Fan J, Cao L et al (2022) A rice single cell transcriptomic atlas defines the developmental trajectories of rice floret and inflorescence meristems. New Phytol 234:494–512. https://doi.org/10.1111/nph.18008

    Article  CAS  PubMed  Google Scholar 

  52. Tanaka W, Ohmori S, Kawakami N, Hirano HY (2021) Flower meristem maintenance by TILLERS ABSENT 1 is essential for ovule development in rice. Development 148:dev199932. https://doi.org/10.1242/dev.199932

    Article  CAS  PubMed  Google Scholar 

  53. Shen C, Li G, Dreni L, Zhang D (2021) Molecular control of carpel development in the grass family. Front Plant Sci 12:635500

    Article  PubMed  PubMed Central  Google Scholar 

  54. Chongloi GL, Prakash S, Vijayraghavan U (2019) Regulation of meristem maintenance and organ identity during rice reproductive development. J Exp Bot 70:1719–1736. https://doi.org/10.1093/jxb/erz046

    Article  CAS  PubMed  Google Scholar 

  55. Coen E, Meyerowitz E (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  CAS  PubMed  Google Scholar 

  56. Colombo L, Franken J, Koetje E, Van Went J, Dons HJM, Angenent GC, Van Tunen AJ (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7:1859–1868. https://doi.org/10.2307/3870193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203. https://doi.org/10.1038/35012103

    Article  CAS  PubMed  Google Scholar 

  58. Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88. https://doi.org/10.1038/nature01741

    Article  CAS  PubMed  Google Scholar 

  59. Thomson B, Wellmer F (2019) Molecular regulation of flower development. In: Grossniklaus U (ed) Plant development and evolution. Current topics in developmental biology, vol 131. Academic Press, New York

    Google Scholar 

  60. Monniaux M, Vandenbussche M (2018) How to evolve a perianth: a review of cadastral mechanisms for perianth identity. Front Plant Sci 9:1573

    Article  PubMed  PubMed Central  Google Scholar 

  61. Causier B, Schwarz-Sommer Z, Davies B (2010) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21:73–79. https://doi.org/10.1016/j.semcdb.2009.10.005

    Article  CAS  PubMed  Google Scholar 

  62. Smaczniak C, Immink RGH, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S et al (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A 109:1560–1565. https://doi.org/10.1073/pnas.1112871109

    Article  PubMed  PubMed Central  Google Scholar 

  63. Theißen G, Melzer R, Ruümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143:3259–3271

    Article  PubMed  Google Scholar 

  64. Hugouvieux V, Silva CS, Jourdain A, Stigliani A, Charras Q, Conn V, Conn SJ, Carles CC, Parcy F, Zubieta C (2018) Tetramerization of MADS family transcription factors SEPALLATA3 and AGAMOUS is required for floral meristem determinacy in Arabidopsis. Nucleic Acids Res 46:4966–4977. https://doi.org/10.1093/nar/gky205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242. https://doi.org/10.1186/1471-2164-8-242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Dreni L, Kater MM (2014) MADS reloaded: evolution of the AGAMOUS subfamily genes. New Phytol 201:717–732. https://doi.org/10.1111/nph.12555

    Article  CAS  PubMed  Google Scholar 

  67. Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano H-Y (2006) Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 18:15–28. https://doi.org/10.1105/tpc.105.037200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dreni L, Pilatone A, Yun D, Erreni S, Pajoro A, Caporali E, Zhang D, Kater MM (2011) Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy. Plant Cell 23:2850–2863. https://doi.org/10.1105/tpc.111.087007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, DePamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8:30–45. https://doi.org/10.1111/j.1525-142X.2006.05073.x

    Article  CAS  PubMed  Google Scholar 

  70. Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166:1011–1023. https://doi.org/10.1534/genetics.166.2.1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Sugiyama S-H, Yasui Y, Ohmori S, Tanaka W, Hirano H-Y (2019) Rice flower development revisited: regulation of carpel specification and flower meristem determinacy. Plant Cell Physiol 60:1284–1295. https://doi.org/10.1093/pcp/pcz020

    Article  CAS  PubMed  Google Scholar 

  72. Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23:515–533. https://doi.org/10.1105/tpc.110.074369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PBF, An G, Colombo L, Kater MM (2007) The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J 52:690–699. https://doi.org/10.1111/j.1365-313X.2007.03272.x

    Article  CAS  PubMed  Google Scholar 

  74. Alvarez J, Smyth DR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126:2377–2386

    Article  CAS  PubMed  Google Scholar 

  75. Alvarez J, Smyth DR (2002) CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. Int J Plant Sci 163:17–41. https://doi.org/10.1086/324178

    Article  CAS  Google Scholar 

  76. Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130:705–718

    Article  CAS  PubMed  Google Scholar 

  77. Morel P, Heijmans K, Ament K, Chopy M, Trehin C, Chambrier P, Bento SR, Bimbo A, Vandenbussche M (2018) The floral C-lineage genes trigger nectary development in Petunia and Arabidopsis. Plant Cell 30:2020–2037. https://doi.org/10.1105/tpc.18.00425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Yun D, Liang W, Dreni L, Yin C, Zhou Z, Kater MM, Zhang D (2013) OsMADS16 genetically interacts with OsMADS3 and OsMADS58 in specifying floral patterning in rice. Mol Plant 6:743–756. https://doi.org/10.1093/mp/sst003

    Article  CAS  PubMed  Google Scholar 

  79. Seok HY, Park HY, Park JI, Lee YM, Lee SY, An G, Moon YH (2010) Rice ternary MADS protein complexes containing class B MADS heterodimer. Biochem Biophys Res Commun 401:598–604. https://doi.org/10.1016/j.bbrc.2010.09.108

    Article  CAS  PubMed  Google Scholar 

  80. Moon YH, Jung JY, Kang HG, An G (1999) Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Mol Biol 40:167–177. https://doi.org/10.1023/A:1026429922616

    Article  CAS  PubMed  Google Scholar 

  81. Yao S-G, Ohmori S, Kimizu M, Yoshida H (2008) Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development. Plant Cell Physiol 49:853–857. https://doi.org/10.1093/pcp/pcn050

    Article  CAS  PubMed  Google Scholar 

  82. Wu F, Shi X, Lin X, Liu Y, Chong K, Theißen G, Meng Z (2017) The ABCs of flower development: mutational analysis of AP1/FUL-like genes in rice provides evidence for a homeotic (A)-function in grasses. Plant J 89:310–324. https://doi.org/10.1111/tpj.13386

    Article  CAS  PubMed  Google Scholar 

  83. Zheng M, Wang Y, Wang Y, Wang C, Ren Y, Lv J, Peng C, Wu T, Liu K, Zhao S et al (2015) DEFORMED FLORAL ORGAN1 (DFO1) regulates floral organ identity by epigenetically repressing the expression of OsMADS58 in rice (Oryza sativa). New Phytol 206:1476–1490. https://doi.org/10.1111/nph.13318

    Article  CAS  PubMed  Google Scholar 

  84. Yan D, Zhang X, Zhang L, Ye S, Zeng L, Liu J, Li Q, He Z (2015) CURVED CHIMERIC PALEA 1 encoding an EMF1-like protein maintains epigenetic repression of OsMADS58 in rice palea development. Plant J 82:12–24. https://doi.org/10.1111/tpj.12784

    Article  CAS  PubMed  Google Scholar 

  85. Schultz EA, Pickett FB, Haughn GW (1991) The FLO10 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers. Plant Cell 3:1221–1237. https://doi.org/10.1105/tpc.3.11.1221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114:599–615. https://doi.org/10.1242/dev.114.3.599

    Article  CAS  PubMed  Google Scholar 

  87. Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378:199–203. https://doi.org/10.1038/378199a0

    Article  CAS  PubMed  Google Scholar 

  88. Krizek BA, Lewis MW, Fletcher JC (2006) RABBIT EARS is a second-whorl repressor of AGAMOUS that maintains spatial boundaries in Arabidopsis flowers. Plant J 45:369–383. https://doi.org/10.1111/j.1365-313X.2005.02633.x

    Article  CAS  PubMed  Google Scholar 

  89. Prunet N, Yang W, Das P, Meyerowitz EM, Jack TP (2017) SUPERMAN prevents class B gene expression and promotes stem cell termination in the fourth whorl of Arabidopsis thaliana flowers. Proc Natl Acad Sci U S A 114:7166–7171. https://doi.org/10.1073/pnas.1705977114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Breuil-Broyer S, Trehin C, Morel P, Boltz V, Sun B, Chambrier P, Ito T, Negrutiu I (2016) Analysis of the Arabidopsis superman allelic series and the interactions with other genes demonstrate developmental robustness and joint specification of male-female boundary, flower meristem termination and carpel compartmentalization. Ann Bot 117:905–923. https://doi.org/10.1093/aob/mcw023

    Article  PubMed  PubMed Central  Google Scholar 

  91. Xu W, Zhu W, Yang L, Liang W, Li H, Yang L, Chen M, Luo Z, Huang G, Duan L et al (2022) SMALL REPRODUCTIVE ORGANS, a SUPERMAN-like transcription factor, regulates stamen and pistil growth in rice. New Phytol 233:1701–1718. https://doi.org/10.1111/nph.17849

    Article  CAS  PubMed  Google Scholar 

  92. Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10:427–435. https://doi.org/10.1016/j.tplants.2005.07.008

    Article  CAS  PubMed  Google Scholar 

  93. Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, DePamphilis CW, Ma H (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223. https://doi.org/10.1534/genetics.104.037770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Dreni L, Ferrándiz C (2022) Tracing the evolution of the SEPALLATA subfamily across angiosperms associated with neo- and sub-functionalization for reproductive and agronomically relevant traits. Plan Theory 11:2934. https://doi.org/10.3390/plants11212934

    Article  CAS  Google Scholar 

  95. Melzer R, Theissen G (2009) Reconstitution of “floral quartets” in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res 37:2723–2736. https://doi.org/10.1093/nar/gkp129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940. https://doi.org/10.1016/j.cub.2004.10.028

    Article  CAS  PubMed  Google Scholar 

  97. Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theißen G, Meng Z (2010) Functional conservation and diversification of class e floral homeotic genes in rice (Oryza sativa). Plant J 61:767–781. https://doi.org/10.1111/j.1365-313X.2009.04101.x

    Article  CAS  PubMed  Google Scholar 

  98. Wu D, Liang W, Zhu W, Chen M, Ferrándiz C, Burton RA, Dreni L, Zhang D (2018) Loss of LOFSEP transcription factor function converts spikelet to leaf-like structures in rice. Plant Physiol 176:1646–1664. https://doi.org/10.1104/pp.17.00704

    Article  CAS  PubMed  Google Scholar 

  99. Ta KN, Sabot F, Adam H, Vigouroux Y, De Mita S, Ghesquière A, Do NV, Gantet P, Jouannic S (2016) MiR2118-triggered phased siRNAs are differentially expressed during the panicle development of wild and domesticated African rice species. Rice 9:10. https://doi.org/10.1186/s12284-016-0082-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Hu Y, Liang W, Yin C, Yang X, Ping B, Li A, Jia R, Chen M, Luo Z, Cai Q et al (2015) Interactions of OsMADS1 with floral homeotic genes in rice flower development. Mol Plant 8:1366–1384

    Article  CAS  PubMed  Google Scholar 

  101. Prasad K, Sriram P, Santhosh Kumar C, Kushalappa K, Vijayraghavan U (2001) Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev Genes Evol 211:281–290. https://doi.org/10.1007/s004270100153

    Article  CAS  PubMed  Google Scholar 

  102. Khanday I, Das S, Chongloi GL, Bansal M, Grossniklaus U, Vijayraghavan U (2016) Genome-wide targets regulated by the OsMADS1 transcription factor reveals its DNA recognition properties. Plant Physiol 172:372–388. https://doi.org/10.1104/pp.16.00789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Dai Z, Wang J, Zhu M, Miao X, Shi Z (2016) OsMADS1 represses MicroRNA172 in elongation of palea/lemma development in rice. Front Plant Sci 7:1891. https://doi.org/10.3389/fpls.2016.01891

    Article  PubMed  PubMed Central  Google Scholar 

  104. Khanday I, Ram Yadav S, Vijayraghavan U (2013) Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways. Plant Physiol 161:1970–1983. https://doi.org/10.1104/pp.112.212423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ren D, Rao Y, Leng Y, Li Z, Xu Q, Wu L, Qiu Z, Xue D, Zeng D, Hu J et al (2016) Regulatory role of OsMADS34 in the determination of glumes fate, grain yield, and quality in rice. Front Plant Sci 7:1853. https://doi.org/10.3389/fpls.2016.01853

    Article  PubMed  PubMed Central  Google Scholar 

  106. Agrawal GK, Abe K, Yamazaki M, Miyao A, Hirochika H (2005) Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Mol Biol 59:125–135. https://doi.org/10.1007/s11103-005-2161-y

    Article  CAS  PubMed  Google Scholar 

  107. Lim J, Moon YH, An G, Jang SK (2000) Two rice MADS domain proteins interact with OsMADS1. Plant Mol Biol 44:513–527. https://doi.org/10.1023/A:1026517111843

    Article  CAS  PubMed  Google Scholar 

  108. Li H, Liang W, Jia R, Yin C, Zong J, Kong H, Zhang D (2010) The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Res 20:299–313. https://doi.org/10.1038/cr.2009.143

    Article  CAS  PubMed  Google Scholar 

  109. Sang X, Li Y, Luo Z, Ren D, Fang L, Wang N, Zhao F, Ling Y, Yang Z, Liu Y et al (2012) CHIMERIC FLORAL ORGANS1, encoding a monocot-specific MADS box protein, regulates floral organ identity in rice. Plant Physiol 160:788–807. https://doi.org/10.1104/pp.112.200980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Rijpkema AS, Zethof J, Gerats T, Vandenbussche M (2009) The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J 60:1–9. https://doi.org/10.1111/j.1365-313X.2009.03917.x

    Article  CAS  PubMed  Google Scholar 

  111. Dreni L, Zhang D (2016) Flower development: the evolutionary history and functions of the AGL6 subfamily MADS-box genes. J Exp Bot 67:1625–1638. https://doi.org/10.1093/jxb/erw046

    Article  CAS  PubMed  Google Scholar 

  112. Viaene T, Vekemans D, Becker A, Melzer S, Geuten K (2010) Expression divergence of the AGL6 MADS domain transcription factor lineage after a core eudicot duplication suggests functional diversification. BMC Plant Biol 10:148. https://doi.org/10.1186/1471-2229-10-148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Moon YH, Kang HC, Jung JY, Jeon JS, Sung SK, An G (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol 120:1193–1203. https://doi.org/10.1104/pp.120.4.1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Favaro R, Immink RGH, Ferioli V, Bernasconi B, Byzova M, Angenent GC, Kater M, Colombo L (2002) Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol Gen Genomics 268:152–159. https://doi.org/10.1007/s00438-002-0746-6

    Article  CAS  Google Scholar 

  115. Lee S, Jeon JS, An K, Moon YH, Lee S, Chung YY, An G (2003) Alteration of floral organ identity in rice through ectopic expression of OsMADS16. Planta 217:904–911. https://doi.org/10.1007/s00425-003-1066-8

    Article  CAS  PubMed  Google Scholar 

  116. DePamphilis CW, Palmer JD, Rounsley S, Sankoff D, Schuster SC, Ammiraju JSS, Barbazuk WB, Chamala S, Chanderbali AS, Determann R et al (2013) The Amborella genome and the evolution of flowering plants. Science 342:1241089. https://doi.org/10.1126/science.1241089

    Article  CAS  Google Scholar 

  117. Gramzow L, Weilandt L, Theißen G (2014) MADS goes genomic in conifers: towards determining the ancestral set of MADS-box genes in seed plants. Ann Bot 114:1407–1429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Hu Y, Wang L, Jia R, Liang W, Zhang X, Xu J, Chen X, Lu D, Chen M, Luo Z et al (2021) Rice transcription factor MADS32 regulates floral patterning through interactions with multiple floral homeotic genes. J Exp Bot 72:2434–2449. https://doi.org/10.1093/jxb/eraa588

    Article  CAS  PubMed  Google Scholar 

  119. Wang H, Zhang L, Cai Q, Hu Y, Jin Z, Zhao X, Fan W, Huang Q, Luo Z, Chen M et al (2015) OsMADS32 interacts with PI-like proteins and regulates rice flower development. J Integr Plant Biol 57:504–513. https://doi.org/10.1111/jipb.12248

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I thank the editors for inviting my contribution, and the European Commission and CSIC for funding (Marie Sklodowska–Curie Individual Fellowship RI No. 661678 “GainGrain” and “convocatoria extensión MSCA IF ERC,” respectively).

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Dreni, L. (2023). The ABC of Flower Development in Monocots: The Model of Rice Spikelet. In: Riechmann, J.L., Ferrándiz, C. (eds) Flower Development . Methods in Molecular Biology, vol 2686. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3299-4_3

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