Abstract
Ghd7, Ghd8, Ghd7.1, and Hd1 are all pleiotropic genes regulating heading date, plant height, and yield in rice. Early studies showed that Hd1 promoted heading under short-day conditions (SD) and delayed heading under long-day conditions (LD). Recent studies found that Hd1 also promoted heading in some genetic backgrounds under LD. In this study, we developed a series of near-isogenic lines for Ghd7, Ghd8, Ghd7.1, and Hd1 in the Zhenshan 97 (ZS97) and Minghui 63 (MH63) backgrounds and recorded their heading dates. In the ZS97 background, Ghd7 alone triggered the conversion of Hd1 function from promoting to suppressing heading under LD. Ghd8 alone and Ghd7.1 alone did not promote but enhanced Ghd7-mediated Hd1 function conversion. In the MH63 background, Ghd7 alone and Ghd7.1 alone did not convert Hd1 function under LD, but they jointly promoted Hd1 function conversion. Conversion of Hd1 function occurred only under LD but not SD. Transcript analysis showed that downregulation or upregulation of Ehd1 and Hd3a by Hd1 in the lines under LD was determined by genetic background. In summary, multiple gene combinations of Ghd7, Ghd7.1, and Ghd8 and unknown genes caused conversion of Hd1 function. Moreover, the different gene combinations had a big difference in photoperiod sensitivities. These findings lay a solid foundation for further unveiling the molecular mechanism of Hd1 function conversion and provide guidance for heading date improvement in rice.
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References
Cho LH, Yoon J, Pasriga R, An G (2016) Homodimerization of Ehd1 is required to induce flowering in rice. Plant Physiol 170:2159–2171
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-Iike gene expression independently of Hd1. Genes Dev 18:926–936
Du A, Tian W, Wei M et al (2017) The DTH8-Hd1 module mediates day-length-dependent regulation of rice flowering. Mol Plant 10:948–961
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42
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
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
Hou X, Zhou J, Liu C, Liu L, Shen L, Yu H (2014) Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nat Commun 5:4601
Hu Y, Li SL, Xing YZ (2019) Lessons from natural variations: artificially induced heading date variations for improvement of regional adaptation in rice. Theor Appl Genet 132:383–394
Kim SK, Park HY, Jang YH, Lee KC, Chung YS, Lee JH, Kim JK (2016) OsNF-YC2 and OsNF-YC4 proteins inhibit flowering under long-day conditions in rice. Planta 243:563–576
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
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
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
Liu X, Yang Y, Hu Y et al (2018) Temporal-specific interaction of NF-YC and CURLY LEAF during the floral transition regulates flowering. Plant Physiol 77:105–114
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
Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF, Mantovani R (2012) The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell 24:4777–4792
Shen GJ, Xing YZ (2014) Two novel QTLs for heading date are identified using a set of chromosome segment substitution lines in rice (Oryza sativa L.). J Gen Genomics 41:659–662
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
Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14:748–750
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
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. Plant Cell 18:2971–2984
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
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
Yan W, Liu H, Zhou X, Li Q, Zhang J, Lu L, Liu T, Liu H, 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 Research 23(7):969–971
Yano M, Katayose Y, Ashikari M 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 12:2473–2484
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
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. Sci Rep 7:5388
Zhang ZH, Wang K, Guo L, Zhu YJ, Fan YY, Cheng SH, Zhuang JY (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, Wang J, Cai M, Zhang H, Wu F, Xu Y, Li C, Cheng Z, Zhang X, Guo X, Sheng P, Wu M, Wang J, Lei C, Wang J, Zhao Z, Wu C, Wang H, Wan J (2017) The OsHAPL1-DTH8-Hd1 complex functions as the transcription regulator to repress heading date in rice. J Exp Bot 68:553–568
Acknowledgments
We would like to appreciate Mr. Jianbo Wang for his excellent management of paddy field.
Funding
This work is supported by the National Natural Science Foundation of China (31601283, 31701054) and the Applied Basis Research Foundation of Wuhan City (2016020101010090).
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ZYZ and BZ are equal contributors. ZYZ and BZ performed the construction of NILs, data collection and analysis, field experiments, and gene expression detection. FXQ and HW contributed to QTLs genotyping. ZXL and YZX designed the research. ZYZ, BZ, and YZX wrote and revised the manuscript. All authors read and approved the final manuscript.
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Zhang, Z., Zhang, B., Qi, F. et al. Hd1 function conversion in regulating heading is dependent on gene combinations of Ghd7, Ghd8, and Ghd7.1 under long-day conditions in rice. Mol Breeding 39, 92 (2019). https://doi.org/10.1007/s11032-019-1001-8
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DOI: https://doi.org/10.1007/s11032-019-1001-8