The CCT domain-containing gene family has large impacts on heading date, regional adaptation, and grain yield in rice

doi:10.1016/S2095-3119(17)61724-6

摘要/Abstract

Abstract: There are 41 members of the CCT (CO, CO-like, and TOC1) domain-containing gene family in rice, which are divided into three subfamilies: COL (CONSTANS-like), CMF (CCT motif family), and PRR (pseudoresponse regulator). The first flowering gene to be isolated by map-based cloning, Heading date 1 (Hd1), which is the orthologue of CO in rice, belongs to COL. The central regulator of plant development, Ghd7, belongs to CMF. The major role in controlling rice distribution to high latitudes, Ghd7.1/PRR37, belongs to PRR. Both of Hd1, Ghd7 and Ghd7.1 simultaneously control grain number, plant height, and the heading date. To date, 13 CCT family genes from these three subfamilies have been shown to regulate flowering. Some of them have pleiotropic effects on grain yield, plant height, and abiotic stresses, and others function as circadian oscillators. There are two independent photoperiod flowering pathways that are mediated by GI-Hd1-Hd3a/RFT and GI-Ehd1-Hd3a/RFT in rice. CCT family genes are involved in both pathways. The latest study reveals that protein interaction between Hd1 and Ghd7 integrates the two pathways. CCT family genes are rich in natural variation because rice cultivars have been subjected to natural and artificial selection for different day lengths in the process of domestication and improvement. Alleles of several crucial CCT family genes such as Hd1, Ghd7, and Ghd7.1 exhibit geographic distribution patterns and are highly associated with yield potentials. In addition, CCT family genes are probably involved in the responses to abiotic stress, which should be emphasized in future work. In general, CCT family genes play important roles in regulating flowering, plant growth, and grain yield. The functional identification and elucidation of the molecular mechanisms of CCT family genes would help construct a flowering regulatory network and maximize their contribution to rice production.

Key words: photoperiod sensitivity , protein interaction , yield potentialgeographic distribution , abiotic stress

. [J]. Journal of Integrative Agriculture, 2017, 16(12): 2686-2697.

ZHANG Jia, HU Yong, XU Li-he, HE Qin, FAN Xiao-wei, XING Yong-zhong. The CCT domain-containing gene family has large impacts on heading date, regional adaptation, and grain yield in rice[J]. Journal of Integrative Agriculture, 2017, 16(12): 2686-2697.

参考文献

Beales J, Turner A, GriYths S, Snape J W, Laurie D A. 2007. A Pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 115, 721–733.

Ben-Naim O, Eshed R, Parnis A, Teper-Bamnolker P, Shalit A, Coupland G, Samach A, Lifschitz E. 2006. The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. The Plant Journal, 46, 462–476.

Cai X N, Ballif J, Endo S, Davis E, Liang M X, Chen D, DeWald D, Kreps J, Zhu T, Wu Y J. 2007. A putative CCAAT-binding transcription factor is a regulator of flowering timing in Arabidopsis. Plant Physiology, 145, 98–105.

Chen J B, Li X Y, Cheng C, Wang Y H, Qin M, Zhu H T, Zeng R Z, Fu X L, Liu Z Q, Zhang G Q. 2014. Characterization of epistatic interaction of QTLs LH8 and EH3 controlling heading date in rice. Scientific Reports, 4, doi: 10.1038/srep04263

Cheng X F, Wang Z Y. 2005. Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. The Plant Journal, 43, 758–768.

Chiang G C K, Barua D, Kramer E M, Amasino R M, Donohue K. 2009. Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proceedings of the National Academy of the Sciences of the United States of America, 106, 11661–11666.

Choi S C, Lee S, Kim S R, Lee Y S, Liu C Y, Cao X F, An G. 2014. Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date 3. Plant Physiology, 164, 1326–1337.

Cockram J, Thiel T, Steuernagel B, Stein N, Taudien S, Bailey P C, O’Sullivan D M. 2012. Genome dynamics explain the evolution of flowering time CCT domain gene families in the Poaceae. PLOS ONE, 7, e45307.

Datta S, Hettiarachchi G H C M, Deng X W, Holm M. 2006. Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth. The Plant Cell, 18, 70–84.

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 & Development, 18, 926–936.

Endo-Higashi N, Izawa T. 2011. Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice. Plant and Cell Physiology, 52, 1083–1094.

Farre E M, Kay S A. 2007. PRR7 protein levels are regulated by light and the circadian clock in Arabidopsis. The Plant Journal, 52, 548–560.

Gao H, Jin M N, Zheng X M, Chen J, Yuan D Y, Xin Y Y, Wang M Q, Huang D Y, Zhang Z, Zhou K N, Sheng P K, Ma J, Ma W W, Deng H F, Jiang L, Liu S J, Wang H Y, Wu C Y, Yuan L P, Wan J M. 2014. Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proceedings of the National Academy of the Sciences of the United States of America, 111, 18399–18399.

Gomez-Ariza J, Galbiati F, Goretti D, Brambilla V, Shrestha R, Pappolla A, Courtois B, Fornara F. 2015. Loss of floral repressor function adapts rice to higher latitudes in Europe. Journal of Experimental Botany, 66, 2027–2039.

Goretti D, Martignago D, Landini M, Brambilla V, Gomez-Ariza J, Gnesutta N, Galbiati F, Collani S, Takagi H, Terauchi R, Mantovani R, Fornara F. 2017. Transcriptional and post-transcriptional mechanisms limit Heading Date 1 (Hd1) function to adapt rice to high latitudes. PLoS Genetics, 13, e1006530.

Gusmaroli G, Tonelli C, Mantovani R. 2002. Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits. Gene, 283, 41–48.

Hassidim M, Harir Y, Yakir E, Kron I, Green R M. 2009. Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta, 230, 481–491.

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.

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. The Plant Journal, 76, 36–46.

Hung H Y, Shannon L M, Tian F, Bradbury P J, Chen C, Flint-Garcia S A, McMullen M D, Ware D, Buckler E S, Doebley J F, Holland J B. 2012. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proceedings of the National Academy of the Sciences of the United States of America, 109, E1913–E1921.

Huo H Q, Wei S H, Bradford K J. 2016. DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proceedings of the National Academy of the Sciences of the United States of America, 113, E2199–E2206.

Ito S, Kawamura H, Niwa Y, Nakamichi N, Yamashino T, Mizuno T. 2009. A genetic study of the Arabidopsis circadian clock with reference to the TIMING OF CAB EXPRESSION 1 (TOC1) gene. Plant and Cell Physiology, 50, 290–303.

Itoh H, Nonoue Y, Yano M, Izawa T. 2010. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nature Genetics, 42, 635–638.

Izawa T. 2007. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. Journal of Experimental Botany, 58, 3091–3097.

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 & Development, 16, 2006–2020.

Kikuchi R, Kawahigashi H, Oshima M, Ando T, Handa H. 2012. The differential expression of HvCO9, a member of the CONSTANS-like gene family, contributes to the control of flowering under short-day conditions in barley. Journal of Experimental Botany, 63, 773–784.

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.

Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K. 2008. Hd3a and RFT1 are essential for flowering in rice. Development, 135, 767–774.

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.

Koo B H, Yoo S C, Park J W, Kwon C T, Lee B D, An G, Zhang Z Y, Li J J, Li Z C, Paek N C. 2013. Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Molecular Plant, 6, 1877–1888.

Kumimoto R W, Adam L, Hymus G J, Repetti P P, Reuber T L, Marion C M, Hempel F D, Ratcliffe O J. 2008. The nuclear factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta, 228, 709–723.

Kumimoto R W, Zhang Y, Siefers N, Holt B F. 2010. NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. The Plant Journal, 63, 379–391.

Ledger S, Strayer C, Ashton F, Kay S A, Putterill J. 2001. Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. The Plant Journal, 26, 15–22.

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. The Plant Journal, 63, 18–30.

Li X, Liu H, Wang M, Liu H, Tian X, Zhou W, Lu T, Wang Z, Chu C, Fang J, Bu Q. 2015. Combinations of Hd2 and Hd4 genes determine rice adaptability to Heilongjiang Province, northern limit of China. Journal of Integrative Plant Biology, 57, 698–707.

Liu H, Dong S Y, Sun D Y, Liu W, Gu F W, Liu Y Z, Guo T, Wang H, Wang J F, Chen Z Q. 2016. CONSTANS-Like 9 (OsCOL9) interacts with receptor for activated C-Kinase 1 (OsRACK1) to regulate blast resistance through salicylic acid and ethylene signaling pathways. PLOS ONE, 11, e0166249.

Liu J H, Shen J Q, Xu Y, Li X H, Xiao J H, Xiong L Z. 2016. Ghd2, a CONSTANS-like gene, confers drought sensitivity through regulation of senescence in rice. Journal of Experimental Botany, 67, 5785–5798.

Lu L, Yan W H, Xue W Y, Shao D, Xing Y Z. 2012. Evolution and association analysis of Ghd7 in rice. PLOS ONE, 7, e34021.

Mantovani R. 1999. The molecular biology of the CCAAT-binding factor NF-Y. Gene, 239, 15–27.

Min J H, Chung J S, Lee K H, Kim C S. 2015. The CONSTANS-like 4 transcription factor, AtCOL4, positively regulates abiotic stress tolerance through an abscisic acid-dependent manner in Arabidopsis. Journal of Integrative Plant Biology, 57, 313–324.

Monfreda C, Ramankutty N, Foley J A. 2008. Farming the planet: 2. Geographic distribution of crop areas, yields, physiological types, and net primary production in the year 2000. Global Biogeochemical Cycles, 22, GB1022.

Morita R, Inoue K, Ikeda K, Hatanaka T, Misoo S, Fukayama H. 2016. Starch content in leaf sheath controlled by CO2-responsive CCT protein is a potential determinant of photosynthetic capacity in rice. Plant and Cell Physiology, 57, 2334–2341.

Murakami M, Matsushika A, Ashikari M, Yamashino T, Mizuno T. 2005. Circadian-associated rice pseudo response regulators (OsPRRs): Insight into the control of flowering time. Bioscience Biotechnology and Biochemistry, 69, 410–414.

Murphy R L, Klein R R, Morishige D T, Brady J A, Rooney W L, Miller F R, Dugas D V, Klein P E, Mullet J E. 2011. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proceedings of the National Academy of Sciences of the United States of America, 108, 16469–16474.

Nemoto Y, Nonoue Y, Yano M, Izawa T. 2016. Hd1,a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. The Plant Journal, 86, 221–233.

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 Physiology, 152, 808–820.

Putterill J, Robson F, Lee K, Simon R, Coupland G. 1995. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell, 80, 847–857.

Robson F, Costa M M, Hepworth S R, Vizir I, Pineiro M, Reeves P H, Putterill J, Coupland G. 2001. Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. The Plant Journal, 28, 619–631.

Samach A, Onouchi H, Gold S E, Ditta G S, Schwarz-Sommer Z, Yanofsky M F, Coupland G. 2000. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613–1616.

Satbhai S B, Yamashino T, Okada R, Nomoto Y, Mizuno T, Tezuka Y, Itoh T, Tomita M, Otsuki S, Aoki S. 2011. Pseudo-response regulator (PRR) homologues of the moss Physcomitrella patens: Insights into the evolution of the PRR family in land plants. DNA Research, 18, 39–52.

Sheng P K, Wu F Q, Tan J J, Zhang H, Ma W W, Chen L P, Wang J C, Wang J, Zhu S S, Guo X P, Wang J L, Zhang X, Cheng Z J, Bao Y Q, Wu C Y, Liu X M, Wan J M. 2016. A CONSTANS-like transcriptional activator, OsCOL13, functions as a negative regulator of flowering downstream of OsphyB and upstream of Ehd1 in rice. Plant Molecular Biology, 92, 209–222.

Strayer C, Oyama T, Schultz T F, Raman R, Somers D E, Mas P, Panda S, Kreps J A, Kay S A. 2000. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science, 289, 768–771.

Sun X H, Zhang Z G, Wu J X, Cui X A, Feng D, Wang K, Xu M, Zhou L, Han X, Gu X F, Lu T G. 2016. The Oryza sativa regulator HDR1 associates with the kinase OsK4 to control photoperiodic flowering. PLoS Genetics, 12, e1005927.

Tamaki S, Matsuo S, Wong H L, Yokoi S, Shimamoto K. 2007. Hd3a protein is a mobile flowering signal in rice. Science, 316, 1033–1036.

Tan J J, Jin M N, Wang J C, Wu F Q, Sheng P K, Cheng Z J, Wang J L, Zheng X M, Chen L P, Wang M, Zhu S S, Guo X P, Zhang X, Liu X M, Wang C M, Wang H Y, Wu C Y, Wan J M. 2016. OsCOL10, a CONSTANS-like gene, functions as a flowering time repressor downstream of Ghd7 in rice. Plant and Cell Physiology, 57, 798–812.

Turner A, Beales J, Faure S, Dunford R P, Laurie D A. 2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science, 310, 1031–1034.

Valverde F. 2011. CONSTANS and the evolutionary origin of photoperiodic timing of flowering. Journal of Experimental Botany, 62, 2453–2463.

Wang H G, Zhang Z L, Li H Y, Zhao X Y, Liu X M, Ortiz M, Lin C T, Liu B. 2013. CONSTANS-LIKE 7 regulates branching and shade avoidance response in Arabidopsis. Journal of Experimental Botany, 64, 1017–1024.

Wang Q X, Xie W B, Xing H K, Yan J, Meng X Z, Li X L, Fu X K, Xu J Y, Lian X M, Yu S B, Xing Y Z, Wang G W. 2015. Genetic architecture of natural variation in rice chlorophyll content revealed by a genome-wide association study. Molecular Plant, 8, 946–957.

Weng X Y, Wang L, Wang J, Hu Y, Du H, Xu C G, Xing Y Z, Li X H, Xiao J H, Zhang Q F. 2014. Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiology, 164, 735–747.

Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G. 2006. CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. The Plant Cell, 18, 2971–2984.

Wu W X, Zheng X M, Lu G W, Zhong Z Z, Gao H, Chen L P, Wu C Y, Wang H J, Wang Q, Zhou K N, Wang J L, Wu F Q, Zhang X, Guo X P, Cheng Z J, Lei C L, Lin Q B, Jiang L, Wang H Y, Ge S, et al. 2013. Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proceedings of the National Academy of the Sciences of the United States of America, 110, 2775–2780.

Xing Y, Xu C, Hua J, Tan Y, Sun X. 2001. Mapping and isolation of quantitative trait loci controlling plant height and heading date in rice. Acta Botanica Sinica, 43, 721–726.

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. Nature Genetics, 40, 761–767.

Yamamoto Y, Sato E, Shimizu T, Nakamich N, Sato S, Kato T, Tabata S, Nagatani A, Yamashino T, Mizuno T. 2003. Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant and Cell Physiology, 44, 1119–1130.

Yan L L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen J L, Echenique V, Dubcovsky J. 2004. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science, 303, 1640–1644.

Yan W H, Liu H Y, Zhou X C, Li Q P, Zhang J, Lu L, Liu T M, Liu H J, Zhang C J, Zhang Z Y, Shen G J, Yao W, Chen H X, Yu S B, Xie W B, Xing Y Z. 2013. Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice. Cell Research, 23, 969–971.

Yan W H, Wang P, Chen H X, Zhou H J, Li Q P, Wang C R, Ding Z H, Zhang Y S, 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. Molecular Plant, 4, 319–330.

Yang Q, Li Z, Li W Q, Ku L X, Wang C, Ye J R, Li K, Yang N, Li Y P, Zhong T, Li J S, Chen Y H, Yan J B, Yang X H, Xu M L. 2013. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proceedings of the National Academy of the Sciences of the United States of America, 110, 16969–16974.

Yang Y, Fu D B, Zhu C M, He Y Z, Zhang H J, Liu T, Li X H, Wu C Y. 2015. The RING-finger ubiquitin ligase HAF1 mediates heading date 1 degradation during photoperiodic flowering in rice. The Plant Cell, 27, 2455–2468.

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. The Plant Cell, 12, 2473–2484.

Yu S B, Li J X, Xu C G, Tan Y F, Li X H, Zhang Q F. 2002. Identification of quantitative trait loci and epistatic interactions for plant height and heading date in rice. Theoretical and Applied Genetics, 104, 619–625.

Zhang J, Zhou X C, Yan W H, Zhang Z Y, Lu L, Han Z M, Zhao H, Liu H Y, Song P, Hu Y, Shen G J, He Q, Guo S B, Gao G Q, Wang G W, Xing Y Z. 2015. Combinations of the Ghd7, Ghd8 and Hd1 genes largely define the ecogeographical adaptation and yield potential of cultivated rice. New Phytologist, 208, 1056–1066.

Zhang L, Li Q P, Dong H J, He Q, Liang L W, Tan C, Han Z M, Yao W, Li G W, Zhao H, Xie W B, Xing Y Z. 2015. Three CCT domain-containing genes were identified to regulate heading date by candidate gene-based association mapping and transformation in rice. Scientific Reports, 5, 7663.

Zhang Y M, Yan Y S, Wang L N, Yang K, Xiao N, Liu Y F, Fu Y P, Sun Z X, Fang R X, Chen X Y. 2012. A novel rice gene, NRR responds to macronutrient deficiency and regulates root growth. Molecular Plant, 5, 63–72.

Zhang Y M, Zhang G, Xiao N, Wang L N, Fu Y P, Sun Z X, Fang R X, Chen X Y. 2013. The rice ‘nutrition response and root growth (NRR)’ gene regulates heading date. Molecular Plant, 6, 585–588.

Zhang Z, Hu W, Shen G, Liu H, Hu Y, Zhou X, Liu T, Xing Y. 2017. Alternative functions of Hd1 in repressing or promoting heading are determined by Ghd7 status under long-day conditions. Scientific Reports, 7, 5388.

Zhang Z H, Wang K, Guo L, Zhu Y J, Fan Y Y, Cheng S H, Zhuang J Y. 2012. Pleiotropism of the photoperiod-insensitive allele of Hd1 on heading date, plant height and yield traits in rice. PLOS ONE, 7, e52538.

Zhu S S, Wang J C, Cai M H, Zhang H, Wu F Q, Xu Y, Li C N, Cheng Z J, Zhang X, Guo X P, Sheng P K, Wu M M, Wang J L, Lei C L, Wang J, Zhao Z C, Wu C Y, Wang H Y, Wan J M. 2017. The OsHAPL1-DTH8-Hd1 complex functions as the transcription regulator to repress heading date in rice. Journal of Experimental Botany, 68, 552–567.