Flower Development and Photoperiodic Control of Flowering in Rice

doi:10.1016/S1672-6308(13)60112-2

Abstract

Abstract:

Floral transition, which is referred to as a plant’s transition from vegetative stage to reproductive stage, is considered to be a critical developmental switch in higher plants, for a timely flowering is a major factor of reproductive success. Endogenous and environmental cues, such as photoperiod, light quality, plant hormones concentrations and temperature, provide information to the plants whether the environment is favorable for flowering. These cues promote, or prevent, flowering through a complex genetic network, mediated by a careful orchestration of temporal and spatial gene expression. One of such cues is photoperiod. Rice (Oryza sativa L.) serves as a powerful model species for the understanding of flowering in higher plants, including flower development and photoperiodic control of flowering. In this review, we overviewed and discussed the flower development and its model. We also overviewed the photoperiodic pathways in rice flowering control, and summarized the pathways at molecular level.

Key words: rice, flowering time gene, floral transition, flower development, photoperiod

XIANG Chao1,2, QU Li-jun1,2, GAO Yong-ming2, SHI Ying-yao1,2 . Flower Development and Photoperiodic Control of Flowering in Rice[J]. RICE SCIENCE, DOI: 10.1016/S1672-6308(13)60112-2 .

References

Albani M C, Coupland G. 2010. Comparative analysis of flowering in annual and perennial plants. Curr Top Dev Biol, 91: 324–341.
Ambrose B A, Lerner D R, Ciceri P, Padilla C M, Yanofsky M F, Schmidt R J. 2000. Molecular and genetic analysis of the Silky1 gene reveals conservation in ?oral organ speci?cation between eudicots and monocots. Mol Cell, 5: 569–579.
Araki T. 2001. Transition from vegetative to reproductive phase. Curr Opin Plant Biol, 4: 63–68.
Arora R, Agarwal P, Ray S, Singh A K, Singh V P, Tyagi A K, Kapoor S. 2007. MADS-box gene family in rice: Genome-wide identi?cation, organization and expression pro?ling during reproductive development and stress. BMC Genom, 8: 242.
B?urle I, Dean C. 2006. The timing of developmental transitions in plants. Cell, 125: 655–664.
Chung Y Y, Kim S R, Finkel D, Yanofsky M F, An G. 1994. Early ?owering and reduced apical dominance result from ectopic expression of a rice MADS box gene. Plant Mol Biol, 26: 657–665.
Ciaf? M, Paolacci A R, Tanzarella O A, Porceddu E. 2011. Molecular aspects of ?ower development in grasses. Sex Plant Reprod, 24: 247–282.
Cockram J, Jones H, Leigh F J, O’Sullivan D, Powell W, Laurie D A, Greenland A J. 2007. Control of flowering time in temperate cereals: Genes, domestication, and sustainable productivity. J Exp Bot, 58: 1231–1244.
Cui R F, Han J K, Zhao S Z, Su K M, Wu F, Du X Q, Xu Q J, 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.
Doi K, Izawa T, Yamanouchi U, Takahiko K, Shimatani Z. 2004. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev, 18: 926–936.
Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk P B, An G, Colombo L, Kater M M. 2007. The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J, 52: 690–699.
Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky M F, Kater M M, Colombo L. 2003. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell, 15: 2603–2611.
Ferrario S, Immink R G, Angenent G C. 2004. Conservation and diversity in ?ower land. Curr Opin Plant Biol, 7: 84–91.
Fornara F, Parenicova L, Falasca G, Pelucchi N, Masiero S, Ciannamea S, Lopez-Dee Z, Altamura M M, Colombo L, Kater M M. 2004. Functional characterization of OsMADS18, a member of AP1/SQUA subfamily of MADS box genes. Plant Physiol, 135: 2207–2219.
Gao X C, Liang W Q, Yin C S, Ji S M, Wang H M, Su X, Guo C C, Kong H Z, Xue H W, Zhang D B. 2010. The SEPALLATA-like gene OsMADS34 is required for rice in?orescence and spikelet development. Plant Physiol, 153: 728–740.
Harmer S L. 2009. The circadian system in higher plants. Ann Rev Plant Biol, 60: 357–377.
Hayama R, Coupland G. 2003. Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol, 6: 13–19.
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. 2003. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature, 422: 719–722.
Hayama R, Coupland G. 2004. The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol, 135: 677–684.
Horigome A, Nagasawa N, Ikeda K, Ito M, Ito J I, Nagato Y. 2009. Rice OPEN BEAK is a negative regulator of class 1 knox genes and a posite regulator of class B ?oral homeotic gene. Plant J, 58: 724–736.
Immink R G H, Kaufmann K, Angement G C. 2010. The ‘ABC’ of MADS domain protein behaviour and interactions. Semin Cell Dev Biol, 21: 87–93.
Ishikawa R, Tamaki S, Yokoi S, Inagaki N, Shinomura T, Takano M, Shimamoto K. 2005. Suppression of the floral activator Hd3a is the principal cause of the night break effect in rice. Plant Cell, 17: 3326–3336.
Ishikawa R, Aoki M, Kurotani K, Yokoi S, Shinomura T, Takano M, Shimamoto K. 2011. Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice ?origen Hd3a and critical day length in rice. Mol Genet Genom, 285: 461–470.
Izawa T, Takahashi Y, Yano M. 2003. Comparative biology comes into bloom: Genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol, 6: 113–120.
Jeon J S, Jang S, Lee S, Nam J, Kin C, Lee S H, Chung Y Y, Kim S R, Lee Y H, Cho Y G, An G. 2000. Leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell, 12: 871–889.
Kater M M, Dreni L, Colombo L. 2006. Functional conservation of MADS-box factors controlling ?oral organ identity in rice and Arabidopsis. J Exp Bot, 57: 3433–3444.
Kim L, Lee S Y, Kim H J, Nam H G, Gyn H. 2007. An OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol, 145: 1484–1494.
Kim S K, Yun C H, Lee J H, Jang Y H, Park H Y, Kim J K. 2008. OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta, 228: 355–365.
Komeda Y. 2004. Genetic regulation of time to flower in Arabidopsis thaliana. Ann Rev Plant Biol, 55: 521–535.
Komiya R, Yokoi S J, Shimamoto K. 2009. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development, 136: 3443–3450.
Kyozuka J, Kobayashi T, Morita M, Shimamoto K. 2000. Spatially and temporally regulated expression of rice MADS-box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol, 41: 710–718.
Lee Y S, Jeong D H, Lee D Y, Yi J, Ryu C H, Kim S L, Jeong H J, Choi S C, Jin P, Yang J, Cho L H, Choi H, An G. 2010. OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J, 63: 18–30.
Levy Y Y, Dean C. 1998. The transition to flowering. Plant Cell, 10: 1973–1990.
Li D J, Yang C H, Li X B, Gan Q, Zhao X F, Zhu L H. 2009. Functional characterization of rice OsDof12. Planta, 229: 1159–1169.
Li H F, Liang W Q, Hu Y, Zhu L, Yin C S, Xu J, Dreni L, Kater M M, Zhang D B. 2011. Rice MADS6 interacts with the ?oral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13 and DROOPING LEAF in specifying ?oral organ identities and meristem fate. Plant Cell, 23: 2536–2552.
Litt A, Kramer M K. 2010. The ABC model and the diversi?cation of ?oral organ identity. Semin Cell Dev Biol, 21: 129–137.
Lopez-Dee Z P, Wittich P, Pe M E, Rigola D, Del Buono I, Sari-Gorla M, Kater M M, Colombo L. 1999. OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet, 25: 237–244.
Malcomber S T, Kellogg E A. 2005. SEPALLATA gene diversi?cation: Brave new whorls. Trend Plant Sci, 10: 427–435.
Matsubara K, Yamanouchi U, Wang Z X, Minobe Y, Izawa T, Yano M. 2008. Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol, 148: 1425–1435.
Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang Z X, Minobe Y, Yano M. 2011. Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J, 66: 603–612.
Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y. 2003. SUPERWOMAN1 and DROOPING LEAF genes control ?oral organ identity in rice. Development, 130: 705–718.
Pelucchi N, Fornara F, Favalli C, Masiero S, Lago C, Pe M E, Colombo L, Kater M M. 2002. Comparative analysis of rice MADS-box genes expressed during ?ower development. Sex Plant Reprod, 15: 113–122.
Peng L T. 2006. Molecular mechanism of flowering time controlling photoperiod pathway in Arabidopsis and rice. Plant Physiol Comm, 42: 1021–1031. (in Chinese with English abstract)
Peng L T, Shi J Y, Li L, Shen G Z, Zhang J L. 2007. Overexpression of transcription factor OsLFL1 delays ?owering time in Oryza sativa. J Plant Physiol, 165: 876–885.
Prasad K, Sriram P, Kumar S C, Kushalappa K, Vijayraghavan U. 2001. Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass organs analogous to sepals. Dev Genes Evol, 211: 281–290.
Ryu C H, Lee S Y, Cho L H, Kim S L, Lee Y S, Choi S C, Jeong H J, Yi J Y, Park S J. 2009. OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ, 32: 1412–1427.
Simpson G G, Gendall A R, Dean C. 1999. When to switch to flowering. Ann Rev Cell Dev Biol, 15: 519–550.
Soltis D E, Chanderbali A S, Kim S, Buzgo M, Soltis P S. 2007. The ABC model and its applicability to basal angiosperms. Ann Bot, 100: 155–163.
Sun C H, Deng X J, Fang J C, Cheng C. 2007. An overview of flowering transition in higher plants. Hereditas, 29: 1182–1190. (in Chinese with English abstract)
Theissen G, Saedler H. 2001. Foral quartets. Nature, 409: 469–471.
Theissen G, Melzer R. 2007. Molecular mechanisms underlying origin and diversi?cation of the angiosperm ?ower. Ann Bot, 100: 603–619.
Thomas B, Vince-Prue D. 1997. Photoperiodism in Plants. London: Academic Press: 85–117.
Thompson B E, Hake S. 2009. Translational biology: From Arabidopsis ?owers to grass in?orescence architecture. Plant Physiol, 149: 38–45.
Tsuji H, Taoka K, Shimamoto K. 2011. Regulation of flowering in rice: Two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol, 14: 45–52.
Wei X J, Xu J F, Guo H N, Jiang L, Chen S H, Yu C, Zhou Z L, Hu P S, Zhai H Q, Wan J M. 2010. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol, 153: 1747–1758.
Wu C Y, You C J, Cai S, Li T L, Chen G X, Byrne M E, Zhang Q F. 2008. RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc Nat Acad Sci USA, 105: 12915–12920.
Xiao J H. Wu C Y, Han B, Xue Y B, Deng X W, Zhang Q F. 2009. Research progress on rice functional genomics in China. Sci China Ser C: Life Sci, 39: 909–924. (in Chinese)
Xu G X, Kong H Z. 2007. Duplication and divergence of ?oral MADS-box genes in grasses: Evidence for the generation and modi?cation of novel regulators. J Integr Plant Biol, 49: 927–939.
Xue W Y, Xing Y Z, Weng X Y, Zhao Y, Tang W J, Wang L, Zhou H J, Yu S B, Xu C G, Li X H, Zhang Q F. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet, 40: 761–767.
Yan W H, Wang P, Chen H X, Yu S B, Xing Y Z, Zhang Q F. 2011. A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant, 4: 319–330.
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis ?owering time gene CONSTANS. Plant Cell, 12: 2473–2484.
Yasuyuki T, Kosuke M, Teshima S, Yokoi H I, Shimamoto K. 2009. Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci USA, 106: 4555–4560.
Yong W D, Chong K, Xu Z H, Tan K, Zhu Z Q. 2000. Genetic control of flowering time in higher plants. Chin Sci Bull, 45: 1633–1642.
Yoshida H, Nagato Y. 2011. Flower development in rice. J Exp Bot, 62: 4719–4730.
Yuan Z, Gao S, Xue D W, Luo D, Li L T, Ding S Y, Yao X, Wilson Z A, Qian Q, Zhang D B. 2009. RETARDED PALEA1 controls palea development and ?oral zygomorphy in rice. Plant Physiol, 149: 235–244.
Zahn L M, Kong H, Leebens-Mack J H, Kim S, Soltis P S. 2005. The evolution of the SEPALLATA subfamily of MADS-box genes: A preangiosperm origin with multiple duplications throughout angiosperm history. Genetics, 169: 2209–2223.

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