Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways

Changhui Sun, Dan Chen, Jun Fang, Pingrong Wang, Xiaojian Deng, Chengcai Chu

PDF(668 KB)
PDF(668 KB)
Protein Cell ›› 2014, Vol. 5 ›› Issue (12) : 889-898. DOI: 10.1007/s13238-014-0068-6
REVIEW
REVIEW

Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways

Author information +
History +

Abstract

Although the molecular basis of flowering time control is well dissected in the long day (LD) plant Arabidopsis, it is still largely unknown in the short day (SD) plant rice. Rice flowering time (heading date) is an important agronomic trait for season adaption and grain yield, which is affected by both genetic and environmental factors. During the last decade, as the nature of florigen was identified, notable progress has been made on exploration how florigen gene expression is genetically controlled. In Arabidopsis expression of certain key flowering integrators such as FLOWERING LOCUS C (FLC) and FLOWERING LOCUS T (FT) are also epigenetically regulated by various chromatin modifications, however, very little is known in rice on this aspect until very recently. This review summarized the advances of both genetic networks and chromatin modifications in rice flowering time control, attempting to give a complete view of the genetic and epigenetic architecture in complex network of rice flowering pathways.

Keywords

rice / flowering time / genetic network / chromatin modifications / Arabidopsis / florigen

Cite this article

Download citation ▾
Changhui Sun, Dan Chen, Jun Fang, Pingrong Wang, Xiaojian Deng, Chengcai Chu. Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways. Protein Cell, 2014, 5(12): 889‒898 https://doi.org/10.1007/s13238-014-0068-6

References

[1]
Andres F, Galbraith DW, Talon M, Domingo C (2009) Analysis of PHOTOPERIOD SENSITIVITY5 sheds light on the role of phytochromes in photoperiodic flowering in rice. Plant Physiol151: 681-690
CrossRef Google scholar
[2]
Brambilla V, Fornara F (2013) Molecular control of flowering in response to day length in rice. J Integr Plant Biol55: 410-418
CrossRef Google scholar
[3]
Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science325: 714-718
CrossRef Google scholar
[4]
Cajlachjan MC (1937) Concerning the hormonal nature of plant development processes. Compt Rend Acad Sci URSS16: 227-230
[5]
Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol61: 579-590
CrossRef Google scholar
[6]
Choi SC, Lee S, Kim S-R, Lee Y-S, Liu C, Cao X, An G (2014) Trithorax group protein OsTrx1 controls flowering time in rice via interaction with Ehd3. Plant Physiol164(3): 1326-1337
CrossRef Google scholar
[7]
Colasanti J, Yuan Z, Sundaresan V (1998) The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell93: 593-603
CrossRef Google scholar
[8]
Colasanti J, Tremblay R, Wong AY, Coneva V, Kozaki A, Mable BK (2006) The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics7: 158
CrossRef Google scholar
[9]
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science316: 1030-1033
CrossRef Google scholar
[10]
Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J29: 1916-1927
CrossRef Google scholar
[11]
Dai X, Ding Y, Tan L, Fu Y, Liu F, Zhu Z, Sun X, Sun X, Gu P, Cai H, Sun C (2012) LHD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon).J Integr Plant Biol54: 790-799
CrossRef Google scholar
[12]
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (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 Dev18: 926-936
CrossRef Google scholar
[13]
Ebana K, Shibaya T, Wu J, Matsubara K, Kanamori H, Yamane H, Yamanouchi U, Mizubayashi T, Kono I, Shomura A, Ito S, Ando T, Hori K, Matsumoto T, Yano M (2011) Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars. Theor Appl Genet122: 1199-1210
CrossRef Google scholar
[14]
Fujino K, Yamanouchi U, Yano M (2013) Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theor Appl Genet126: 611-618
CrossRef Google scholar
[15]
Gao H, Zheng XM, Fei G, Chen J, Jin M, Ren Y, Wu W, Zhou K, Sheng P, Zhou F, Jiang L, Wang J, Zhang X, Guo X, Wang JL, Cheng Z, Wu C, Wang H, Wan JM (2013) Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet9: e1003281
CrossRef Google scholar
[16]
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature422: 719-722
CrossRef Google scholar
[17]
He Y (2009) Control of the transition to flowering by chromatin modifications. Mol Plant2: 554-564
CrossRef Google scholar
[18]
Hori K, Kataoka T, Miura K, Yamaguchi M, Saka N, Nakahara T, Sunohara Y, Ebana K, Yano M (2012) Variation in heading date conceals quantitative trait loci for other traits of importance in breeding selection of rice. Breed Sci62: 223-234
CrossRef Google scholar
[19]
Hori K, Ogiso-Tanaka E, Matsubara K, Yamanouchi U, Ebana K, Yano M (2013) Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response. Plant J76: 36-46
[20]
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 florigen Hd3a and critical day length in rice. Mol Genet Genomics285: 461-470
CrossRef Google scholar
[21]
Itoh H, Izawa T (2013) The coincidence of critical day length recognition for florigen gene expression and floral transition under long-day conditions in rice. Mol Plant6: 635-649
CrossRef Google scholar
[22]
Itoh H, Nonoue Y, Yano M, Izawa T (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat Genet42: 635-638
CrossRef Google scholar
[23]
Izawa T (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot58: 3091-3097
CrossRef Google scholar
[24]
Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev16: 2006-2020
CrossRef Google scholar
[25]
Kim SL, Lee S, Kim HJ, Nam HG, An G (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol145: 1484-1494
CrossRef Google scholar
[26]
Kim SK, Yun CH, Lee JH, Jang YH, Park HY, Kim JK (2008) OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta228: 355-365
CrossRef Google scholar
[27]
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under shortday conditions. Plant Cell Physiol43: 1096-1105
CrossRef Google scholar
[28]
Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development135: 767-774
CrossRef Google scholar
[29]
Komiya R, Yokoi S, Shimamoto K (2009) A gene network for longday flowering activates RFT1 encoding a mobile flowering signal in rice. Development136: 3443-3450
CrossRef Google scholar
[30]
Koo BH, Yoo SC, Park JW, Kwon CT, Lee BD, An G, Zhang Z, Li J, Li Z, Paek NC (2013) Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant6: 1877-1888
CrossRef Google scholar
[31]
Kwon CT, Yoo SC, Koo BH, Cho SH, Park JW, Zhang Z, Li J, Li Z, Paek NC (2013) Natural variation in Early flowering1 contributes to early flowering in japonica rice under long days. Plant Cell Environ37: 101-112
CrossRef Google scholar
[32]
Lee S, Kim J, Han JJ, Han MJ, An G (2004) Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/ AGL20) ortholog in rice. Plant J38: 754-764
CrossRef Google scholar
[33]
Lee YS, Jeong DH, Lee DY, Yi J, Ryu CH, Kim SL, Jeong HJ, Choi SC, Jin P, Yang J, Cho LH, Choi H, An G (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J63: 18-30
[34]
Li D, Yang C, Li X, Gan Q, Zhao X, Zhu L (2009) Functional characterization of rice OsDof12. Planta229: 1159-1169
CrossRef Google scholar
[35]
Li W, Han Y, Tao F, Chong K (2011) Knockdown of SAMS genes encoding S-adenosyl-l-methionine synthetases causes methylation alterations of DNAs and histones and leads to late flowering in rice. J Plant Physiol168: 1837-1843
CrossRef Google scholar
[36]
Lin S, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet96: 997-1003
CrossRef Google scholar
[37]
Lin HX, Yamamoto T, Sasaki T, Yano M (2000) Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines. Theor Appl Genet101: 1021-1028
CrossRef Google scholar
[38]
Lin H, Liang Z-W, Sasaki T, Yano M (2003) Fine mapping and characterization of quantitative trait loci Hd4 and Hd5 controlling heading date in rice. Breed Sci53: 51-59
CrossRef Google scholar
[39]
Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol61: 395-420
CrossRef Google scholar
[40]
Liu T, Liu H, Zhang H, Xing Y (2013) Validation and characterization of Ghd7.1, a major quantitative trait locus with pleiotropic effects on spikelets per panicle, plant height, and heading date in rice (Oryza sativa L.). J Integr Plant Biol55: 917-927
[41]
Matsubara K, Yamanouchi U, Wang ZX, Minobe Y, Izawa T, Yano M (2008) Ehd2, a rice ortholog of the maize ID1 gene, promotes flowering by upregulating Ehd1. Plant Physiol148: 1425-1435
CrossRef Google scholar
[42]
Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang ZX, Minobe Y, Yano M (2011) Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J66: 603-612
CrossRef Google scholar
[43]
Matsubara K, Ogiso-Tanaka E, Hori K, Ebana K, Ando T, Yano M (2012) Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol53: 709-716
CrossRef Google scholar
[44]
Ng DW, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: structure, function and regulation. Biochim Biophys Acta1769: 316-329
CrossRef Google scholar
[45]
Nonoue Y, Fujino K, Hirayama Y, Yamanouchi U, Lin SY, Yano M (2008) Detection of quantitative trait loci controlling extremely early heading in rice. Theor Appl Genet116: 715-722
CrossRef Google scholar
[46]
Ogiso E, Takahashi Y, Sasaki T, Yano M, Izawa T (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol152: 808-820
CrossRef Google scholar
[47]
Park SJ, Kim SL, Lee S, Je BI, Piao HL, Park SH, Kim CM, Ryu CH, Park SH, Xuan YH, Colasanti J, An G, Han CD (2008) Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J56: 1018-1029
CrossRef Google scholar
[48]
Peng LT, Shi ZY, Li L, Shen GZ, Zhang JL (2007) Ectopic expression of OsLFL1 in rice represses Ehd1 by binding on its promoter. Biochem Biophys Res Commun360: 251-256
CrossRef Google scholar
[49]
Peng LT, Shi ZY, Li L, Shen GZ, Zhang JL (2008) Overexpression of transcription factor OsLFL1 delays flowering time in Oryza sativa. J Plant Physiol165: 876-885
CrossRef Google scholar
[50]
Ryu CH, Lee S, Cho LH, Kim SL, Lee YS, Choi SC, Jeong HJ, Yi J, Park SJ, Han CD, An G (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ32: 1412-1427
CrossRef Google scholar
[51]
Saito H, Ogiso-Tanaka E, Okumoto Y, Yoshitake Y, Izumi H, Yokoo T, Matsubara K, Hori K, Yano M, Inoue H, Tanisaka T (2012) Ef7 encodes an ELF3-like protein and promotes rice flowering by negatively regulating the floral repressor gene Ghd7 under both short- and long-day conditions. Plant Cell Physiol53: 717-728
CrossRef Google scholar
[52]
Salome PA, Bomblies K, Laitinen RA, Yant L, Mott R, Weigel D (2011) Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics188: 421-433
CrossRef Google scholar
[53]
Shibaya T, Nonoue Y, Ono N, Yamanouchi U, Hori K, Yano M (2011) Genetic interactions involved in the inhibition of heading by heading date QTL, Hd2 in rice under long-day conditions. Theor Appl Genet123: 1133-1143
CrossRef Google scholar
[54]
Sui P, Shi J, Gao X, Shen WH, Dong A (2012) H3K36 methylation is involved in promoting rice flowering. Mol Plant6: 975-977
CrossRef Google scholar
[55]
Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F, Qian Q, Cao X, Chu C (2012) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell24: 3235-3247
CrossRef Google scholar
[56]
Takahashi Y, Shimamoto K (2011) Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice. Genes Genet Syst86: 175-182
CrossRef Google scholar
[57]
Takahashi Y, Shomura A, Sasaki T, Yano M (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA98: 7922-7927
CrossRef Google scholar
[58]
Takahashi Y, Teshima KM, Yokoi S, Innan H, 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 USA106: 4555-4560
CrossRef Google scholar
[59]
Takimoto A, Ikeda K (1961) Effect of twilight on photoperiodic induction in some short day plants. Plant Cell Physiol2: 213-229
[60]
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science316: 1033-1036
CrossRef Google scholar
[61]
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 Biol14: 45-52
CrossRef Google scholar
[62]
Tsuji H, Taoka K, Shimamoto K (2013) Florigen in rice: complex gene network for florigen transcription, florigen activation complex, and multiple functions. Curr Opin Plant Biol16: 228-235
CrossRef Google scholar
[63]
Wang J, Hu J, Qian Q, Xue HW (2012) LC2 and OsVIL2 promote rice flowering by photoperoid-induced epigenetic silencing of OsLF. Mol Plant6: 514-527
CrossRef Google scholar
[64]
Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol153: 1747-1758
CrossRef Google scholar
[65]
Wu C, You C, Li C, Long T, Chen G, Byrne ME, Zhang Q (2008) RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc Natl Acad Sci USA105: 12915-12920
CrossRef Google scholar
[66]
Wu W, Zheng XM, Lu G, Zhong Z, Gao H, Chen L, Wu C, Wang HJ, Wang Q, Zhou K, Wang JL, Wu F, Zhang X, Guo X, Cheng Z, Lei C, Lin Q, Jiang L,Wang H, Ge S, Wan J (2013) Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc Natl Acad Sci USA110: 2775-2780
CrossRef Google scholar
[67]
Xu L, Zhao Z, Dong A, Soubigou-Taconnat L, Renou JP, Steinmetz A, Shen WH (2008) Di- and tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol Cell Biol28: 1348-1360
CrossRef Google scholar
[68]
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet40: 761-767
CrossRef Google scholar
[69]
Yamamoto T, Lin H, Sasaki T, Yano M (2000) Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny. Genetics154: 885-891
[70]
Yan WH, Wang P, Chen HX, Zhou HJ, Li QP, Wang CR, Ding ZH, Zhang YS, Yu SB, Xing YZ, Zhang QF (2011) A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant4: 319-330
CrossRef Google scholar
[71]
Yan W, Liu H, Zhou X, Li Q, Zhang J, Lu L, Liu T, Zhang C, Zhang Z, Shen G, Yao W, Chen H, Yu S, Xie W, Xing Y (2013) Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice. Cell Res23: 969-971
CrossRef Google scholar
[72]
Yang J, Lee S, Hang R, Kim SR, Lee YS, Cao X, Amasino R, An G (2012) OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J73: 566-578
CrossRef Google scholar
[73]
Yang Y, Peng Q, Chen GX, Li XH, Wu CY (2013) OsELF3 is involved in circadian clock regulation for promoting flowering under longday conditions in rice. Mol Plant6: 202-215
CrossRef Google scholar
[74]
Yano M, Harushima Y, Nagamura Y, Kurata N, Minobe Y, Sasaki T (1997) Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor Appl Genet95: 1025-1032
CrossRef Google scholar
[75]
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell12: 2473-2484
CrossRef Google scholar
[76]
Zhao Z, Yu Y, Meyer D, Wu C, Shen WH (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat Cell Biol7: 1256-1260
CrossRef Google scholar
[77]
Zhao XL, Shi ZY, Peng LT, Shen GZ, Zhang JL (2011) An atypical HLH protein OsLF in rice regulates flowering time and interacts with OsPIL13 and OsPIL15. Nat Biotechnol28: 788-797
[78]
Zhao J, Huang X, Ouyang X, Chen W, Du A, Zhu L, Wang S, Deng XW, Li S (2012) OsELF3-1, an ortholog of Arabidopsis early flowering 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS ONE7: e43705
CrossRef Google scholar

RIGHTS & PERMISSIONS

2014 This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
AI Summary AI Mindmap
PDF(668 KB)

Accesses

Citations

Detail

Sections
Recommended

/