Abstract
Key message
A novel Hd3a allele strongly promoting rice heading date was identified, and it functions through florigen activation complex (FAC) and was selected during the spread of rice cultivation to high-latitude areas.
Abstract
Heading date is a critical agronomic trait for rice that determines the utilization of light and temperature conditions and thereby affects grain yield. Rice is a short day (SD) plant, and its photoperiodic information is processed by complex pathways and integrated by florigens to control flowering. In this study, we identified a novel allele for the florigen gene Heading date 3a (Hd3a), characterized by a C435G substitution in its coding region, by a genome-wide association study (GWAS) approach in a panel of 199 high-latitude japonica rice varieties. The C435G substitution induces plants to flower 10 days earlier in high-latitude area (long day condition). Then, we mutated C435 to G in Hd3a by prime editing and found the point mutation plants flowered 12 days earlier. Further molecular experiments showed the novel Hd3a protein can interact with GF14b protein and increase the expression of OsMADS14, the output gene of florigen activation complex (FAC). Molecular signatures of selection indicated that the novel Hd3a allele was selected during the process of rice cultivation expansion into high-latitude areas. Collectively, these results provide new insights into heading date regulation in high-latitude areas and advance improvements to rice adaptability to enhance crop yield.
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References
Ahn JH, Miller D, Winter VJ, Banfield MJ, Jeong HL, So YY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614. https://doi.org/10.1038/sj.emboj.7600950
Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, Liu DR (2019) Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576:149–157. https://doi.org/10.1038/s41586-019-1711-4
Bandillo N, Raghavan C, Muyco PA, Sevilla MAL, Lobina IT, Dilla-Ermita CJ, Tung CW, McCouch S, Thomson M, Mauleon R, Kumar Singh R, Gregorio G, Redoña E, Leung H (2013) Multi-parent advanced generation inter-cross (MAGIC) populations in rice: progress and potential for genetics research and breeding. Rice 6:11
Brambilla V, Martignago D, Goretti D, Cerise M, Somssich M, de Rosa M, Galbiati F, Shrestha R, Lazzaro F, Simon R, Fornara F (2017) Antagonistic transcription factor complexes modulate the floral transition in rice. Plant Cell 29:2801–2816. https://doi.org/10.1105/tpc.17.00645
Cai M, Zhu S, Wu M, Zheng X, Wang J, Zhou L, Zheng T, Cui S, Zhou S, Li C, Zhang H, Chai J, Zhang X, Jin X, Cheng Z, Zhang X, Lei C, Ren Y, Lin Q, Guo X, Zhao L, Wang J, Zhao Z, Jiang L, Wang H, Wan J (2021) DHD4, a Constans-like family transcription factor, delays heading date by affecting the formation of the FAC complex in rice. Mol Plant 14:330–343. https://doi.org/10.1016/j.molp.2020.11.013
Cavanagh C, Morell M, Mackay I, Powell W (2008) From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr Opin Plant Biol 11:215–221. https://doi.org/10.1016/j.pbi.2008.01.002
Chen J-Y, Guo L, Ma H, Chen Y-Y, Zhang H-W, Ying J-Z, Zhuang J-Y (2014) Fine mapping of qHd1, a minor heading date QTL with pleiotropism for yield traits in rice (Oryza sativa L.). Theor Appl Genet 127:2515–2524. https://doi.org/10.1007/s00122-014-2395-7
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. https://doi.org/10.1101/gad.1189604
Gao H, Jin M, Zheng X-M, Chen J, Yuan D, Xin Y, Wang M, Huang D, Zhang Z, Zhou K, Sheng P, Ma J, Ma W, Deng H, Jiang L, Liu S, Wang H, Wu C, Yuan L, Wan J (2014) Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci 111:16337–16342. https://doi.org/10.1073/pnas.1418204111
Gao H, Zheng X-M, 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 J-L, Cheng Z, Wu C, Wang H, Wan J-M (2013) Ehd4 encodes a novel and oryza -genus-specific regulator of photoperiodic flowering in rice. PLOS Genet 9:e1003281. https://doi.org/10.1371/journal.pgen.1003281
Goretti D, Martignago D, Landini M, Brambilla V, Gómez-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 Genet 13:e1006530. https://doi.org/10.1371/journal.pgen.1006530
Han Z, Hu G, Liu H, Liang F, Yang L, Zhao H, Zhang Q, Li Z, Zhang Q, Xing Y (2020) Bin-based genome-wide association analyses improve power and resolution in QTL mapping and identify favorable alleles from multiple parents in a four-way MAGIC rice population. Theor Appl Genet 133:59–71. https://doi.org/10.1007/s00122-019-03440-y
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. https://doi.org/10.1111/tpj.12268
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. https://doi.org/10.1101/gad.999202
Kajiya-Kanegae H, Ohyanagi H, Ebata T, Tanizawa Y, Onogi A, Sawada Y, Hirai MY, Wang Z-X, Han B, Toyoda A, Fujiyama A, Iwata H, Tsuda K, Suzuki T, Nosaka-Takahashi M, Nonomura K, Nakamura Y, Kawamoto S, Kurata N, Sato Y (2021) Oryzagenome2.1: database of diverse genotypes in wild oryza Species. Rice 14:24. https://doi.org/10.1186/s12284-021-00468-x
Kaneko-Suzuki M, Kurihara-Ishikawa R, Okushita-Terakawa C, Kojima C, Nagano-Fujiwara M, Ohki I, Tsuji H, Shimamoto K, Taoka K-I (2018) TFL1-like proteins in rice antagonize rice FT-like protein in inflorescence development by competition for complex formation with 14–3-3 and FD. Plant Cell Physiol 59:458–468. https://doi.org/10.1093/pcp/pcy021
Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida H, Nagamura Y, Kyozuka J (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-Like MADS box genes and PAP2, a sepallata mads box gene. Plant Cell 24:1848–1859. https://doi.org/10.1105/tpc.112.097105
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
Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774. https://doi.org/10.1242/dev.008631
Lee S, Kim J, Han J-J, Han M-J, 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. https://doi.org/10.1111/j.1365-313X.2004.02082.x
Li J-Y, Wang J, Zeigler RS (2014) The 3,000 rice genomes project: new opportunities and challenges for future rice research. GigaScience 3:8. https://doi.org/10.1186/2047-217X-3-8
Li X, Liu H, Wang M, Liu H, Tian X, Zhou W, Lü 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. J Integr Plant Biol 57:698–707. https://doi.org/10.1111/jipb.12326
Li N, Zheng H, Cui J, Wang J, Liu H, Sun J, Liu T, Zhao H, Lai Y, Zou D (2019) Genome-wide association study and candidate gene analysis of alkalinity tolerance in japonica rice germplasm at the seedling stage. Rice 12:24. https://doi.org/10.1186/s12284-019-0285-y
Lippert C, Listgarten J, Liu Y, Kadie CM, Davidson RI, Heckerman D (2011) FaST linear mixed models for genome-wide association studies. Nat Methods 8:833–835. https://doi.org/10.1038/nmeth.1681
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. https://doi.org/10.1104/pp.108.125542
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: Ehd3 is critical promoter of rice flowering. Plant J 66:603–612. https://doi.org/10.1111/j.1365-313X.2011.04517.x
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. https://doi.org/10.1093/pcp/pcs028
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. Plant J 86:221–233. https://doi.org/10.1111/tpj.13168
Shrestha R, Gómez-Ariza J, Brambilla V, Fornara F (2014) Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals. Ann Bot 103:1165–1172. https://doi.org/10.1093/aob/mcu032
Simes RJ (1986) An improved bonferroni procedure for multiple tests of significance. Biometrika 73:751–754. https://doi.org/10.1093/biomet/73.3.751
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. https://doi.org/10.1105/tpc.112.101436
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 106:4555–4560
Takano M, Inagaki N, Xie X, Kiyota S, Baba-Kasai A, Tanabata T, Shinomura T (2009) Phytochromes are the sole photoreceptors for perceiving red/far-red light in rice. Proc Natl Acad Sci 106:14705–14710. https://doi.org/10.1073/pnas.0907378106
Tamaki S, Tsuji H, Matsumoto A, Fujita A, Shimatani Z, Terada R, Sakamoto T, Kurata T, Shimamoto K (2015) FT-like proteins induce transposon silencing in the shoot apex during floral induction in rice. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1417623112
Taoka K, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S, Ogaki Y, Shimada C, Nakagawa A, Kojima C, Shimamoto K (2011) 14–3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476:332–335. https://doi.org/10.1038/nature10272
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. https://doi.org/10.1016/j.pbi.2010.08.016
Tsuji H, Nakamura H, Taoka K, Shimamoto K (2013) Functional diversification of fd transcription factors in rice, components of florigen activation complexes. Plant Cell Physiol 54:385–397. https://doi.org/10.1093/pcp/pct005
Xiao N, Pan C, Li Y, Wu Y, Cai Y, Lu Y, Wang R, Yu L, Shi W, Kang H, Zhu Z, Huang N, Zhang X, Chen Z, Liu J, Yang Z, Ning Y, Li A (2021) Genomic insight into balancing high yield, good quality, and blast resistance of japonica rice. Genome Biol 22:283. https://doi.org/10.1186/s13059-021-02488-8
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. https://doi.org/10.1038/ng.143
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. https://doi.org/10.1093/mp/ssq070
Yan W, Liu H, Zhou X, Li Q, Zhang J, Lu L, Liu T, Liu H, Zhang C, Zhang Z et al (2013) Natural variation in Ghd7. 1 plays an important role in grain yield and adaptation in rice. Cell Res 23:969–971
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y et al (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483
Yano K, Yamamoto E, Aya K, Takeuchi H, Lo P, Hu L, Yamasaki M, Yoshida S, Kitano H, Hirano K, Matsuoka M (2016) Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat Genet 48:927–934. https://doi.org/10.1038/ng.3596
Zhang J, Zhou X, Yan W, Zhang Z, Lu L, Han Z, Zhao H, Liu H, Song P, Hu Y, Shen G, He Q, Guo S, Gao G, Wang G, Xing Y (2015) Combinations of the Ghd7, Ghd8 and Hd1 genes largely define the ecogeographical adaptation and yield potential of cultivated rice. New Phytol 208:1056–1066. https://doi.org/10.1111/nph.13538
Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM, Bustamante CD, McCouch SR (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467. https://doi.org/10.1038/ncomms1467
Zhao G, Wang J, Chen X, Sha H, Liu X, Han Y, Qiu G, Zhang F, Fang J (2022) OsASHL1 and OsASHL2, two members of the compass-like complex, control floral transition and plant development in rice. J Genet Genomics Yi Chuan Xue Bao 49:870–880. https://doi.org/10.1016/j.jgg.2022.02.026
Zong W, Ren D, Huang M, Sun K, Feng J, Zhao J, Xiao D, Xie W, Liu S, Zhang H, Qiu R, Tang W, Yang R, Chen H, Xie X, Chen L, Liu Y, Guo J (2021) Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading. New Phytol 229:1635–1649. https://doi.org/10.1111/nph.16946
Acknowledgements
We thank Dr Jinxing Guo (College of Life Sciences, South China Agricultural University, China) for kindly providing the Hd3a vector.
Funding
This work was supported by grants from the National Natural Science Foundation of China (U20A2025, 31900423), the Postdoctoral researchers settled in Heilongjiang scientific research start fund (LBH-Q21198), High tech industrialization of scientific and technological cooperation between Jilin Province and Chinese Academy of Sciences(2021SYHZ0032), and Key R&D Program Project of Heilongjiang Province (GA21B014).
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ZM H performed the experiments, analyzed the data and wrote the paper. XL L and HJ S performed the experiments. J L and CZ Z revised the manuscript, JG W, HL Z and DT Z provided germplasm resources, J F conceived the project, designed the research and wrote the paper.
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Han, Z., Lei, X., Sha, H. et al. Adaptation to high latitudes through a novel allele of Hd3a strongly promoting heading date in rice. Theor Appl Genet 136, 141 (2023). https://doi.org/10.1007/s00122-023-04391-1
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DOI: https://doi.org/10.1007/s00122-023-04391-1