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

Protein and Cell

Volumn 5, Issue 12, 2014, Pages 889-898

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

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

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

Indexed keywords

FLORIGEN; S ADENOSYLMETHIONINE; ARABIDOPSIS PROTEIN; CHROMATIN; FLF PROTEIN, ARABIDOPSIS; FT PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN;

AGRONOMIC TRAIT; ARABIDOPSIS; ARTICLE; CHROMATIN; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; FLOWERING; GENE; GENE MUTATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; GRAIN YIELD; HD3A GENE; HEREDITY; MOLECULAR GENETICS; NONHUMAN; PROTEIN EXPRESSION; RFT1 GENE; RICE; CHEMISTRY; FLOWER; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORYZA; PHENOTYPE; TIME;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; EPIGENESIS, GENETIC; FLORIGEN; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; MADS DOMAIN PROTEINS; ORYZA; PHENOTYPE; TIME FACTORS;

EID: 84916888441     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-014-0068-6     Document Type: Article

References (78)

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 Physiol 151:681–690
2. Brambilla V, Fornara F (2013) Molecular control of flowering in response to day length in rice. J Integr Plant Biol 55:410–418
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. Science 325:714–718
4. Cajlachjan MC (1937) Concerning the hormonal nature of plant development processes. Compt Rend Acad Sci URSS 16:227–230
5. Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590
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 Physiol 164(3):1326–1337
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. Cell 93:593–603
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 Genomics 7:158
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. Science 316:1030–1033
10. Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29:1916–1927
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 Biol 54:790–799
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 Dev 18:926–936
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 Genet 122:1199–1210
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 Genet 126:611–618
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 Genet 9:e1003281
16. 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
17. He Y (2009) Control of the transition to flowering by chromatin modifications. Mol Plant 2:554–564
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 Sci 62:223–234
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 J 76:36–46
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 Genomics 285:461–470
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 Plant 6:635–649
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 Genet 42:635–638
23. Izawa T (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58:3091–3097
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 Dev 16:2006–2020
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 Physiol 145:1484–1494
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. Planta 228:355–365
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 short-day conditions. Plant Cell Physiol 43:1096–1105
28. Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774
29. Komiya R, Yokoi S, Shimamoto K (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–3450
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 Plant 6:1877–1888
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 Environ 37:101–112
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 J 38:754–764
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 J 63:18–30
34. Li D, Yang C, Li X, Gan Q, Zhao X, Zhu L (2009) Functional characterization of rice OsDof12. Planta 229:1159–1169
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 Physiol 168:1837–1843
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 Genet 96:997–1003
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 Genet 101:1021–1028
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 Sci 53:51–59
39. Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420
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 Biol 55:917–927
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 Physiol 148:1425–1435
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 J 66:603–612
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 Physiol 53:709–716
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 Acta 1769:316–329
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 Genet 116:715–722
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 Physiol 152:808–820
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 J 56:1018–1029
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 Commun 360:251–256
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 Physiol 165:876–885
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 Environ 32:1412–1427
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 Physiol 53:717–728
52. Salome PA, Bomblies K, Laitinen RA, Yant L, Mott R, Weigel D (2011) Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics 188:421–433
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 Genet 123:1133–1143
54. Sui P, Shi J, Gao X, Shen WH, Dong A (2012) H3K36 methylation is involved in promoting rice flowering. Mol Plant 6:975–977
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 Cell 24:3235–3247
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 Syst 86:175–182
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 USA 98:7922–7927
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 USA 106:4555–4560
59. Takimoto A, Ikeda K (1961) Effect of twilight on photoperiodic induction in some short day plants. Plant Cell Physiol 2:213–229
60. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036
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 Biol 14:45–52
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 Biol 16:228–235
63. Wang J, Hu J, Qian Q, Xue HW (2012) LC2 and OsVIL2 promote rice flowering by photoperoid-induced epigenetic silencing of OsLF. Mol Plant 6:514–527
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 Physiol 153:1747–1758
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 USA 105:12915–12920
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 USA 110:2775–2780
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 Biol 28:1348–1360
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 Genet 40:761–767
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. Genetics 154:885–891
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 Plant 4:319–330
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 Res 23:969–971
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 J 73:566–578
73. Yang Y, Peng Q, Chen GX, Li XH, Wu CY (2013) OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice. Mol Plant 6:202–215
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 Genet 95:1025–1032
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 Cell 12:2473–2484
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 Biol 7:1256–1260
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 Biotechnol 28:788–797
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 ONE 7:e43705