Abstract
A rice hybrid is the product of a cross between two genetically distinct inbred lines. Owing to yield heterosis in rice hybrids, hybrid rice breeding has been developed and widely used in agriculture. In some cases, the hybrid F1 lines show extremely late flowering. However, the genetic basis of the phenomenon is not very clear. In this study, two hybrids were found to have heading date of ~ 130 days, which was much later than their inbred parents. To elucidate the underlying mechanism, mapping populations consisting ~ 2000 F2 individuals were developed, and eight pools were created based on the flowering time of the F2 individuals. Whole genome deep sequencing of the parental lines and the eight pools enabled the identification of two major loci underlying heading date, on chromosome 6 and 8, respectively. Follow-up PCR amplification and Sanger sequencing showed Hd1 (Heading date1) and Ghd8/DTH8 (Grain number, plant height and heading date 8) were probably the causal genes on the two loci. The female parent had the genotype Hd1WT ghd81bp-del while the male parents had the genotype hd14bp-del Ghd8WT. Furthermore, genotypes of F2 individuals at Hd1 and Ghd8 were investigated to estimate the genetic effects of different genotype combinations. The result showed that dominance complementation effects of the two genes leaded to extremely late flowering in the F1 hybrid crosses with the genotype Hd1WT/4bp-del Ghd8WT/1bp-del. Taken together, this study lays a foundation for further functional validation and breeding utilization of important flowering genes in genetic improvements of hybrid rice.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The raw DNA sequencing data for the samples are deposited in the European Nucleotide Archive under accession number PRJEB39206.
References
Balaji Suresh P, Srikanth B, Hemanth Kishore V, Subhakara Rao I, Vemireddy LR, Dharika N, Sundaram RM, Ramesha MS, Sambasiva Rao KRS, Viraktamath BC, Neeraja CN (2012) Fine mapping of Rf3 and Rf4 fertility restorer loci of WA-CMS of rice (Oryza sativa L.) and validation of the developed marker system for identification of restorer lines. Euphytica 187:421–435. https://doi.org/10.1007/s10681-012-0737-6
Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966. https://doi.org/10.1093/aob/mcm121
Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci U S A 109:2654–2659. https://doi.org/10.1073/pnas.1121374109
Du A, Tian W, Wei M, Yan W, He H, Zhou D, Huang X, Li S, Ouyang X (2017) The DTH8-Hd1 module mediates day-length-dependent regulation of rice flowering. Mol Plant 10:948–961. https://doi.org/10.1016/j.molp.2017.05.006
Hu R, Zhao M, Zheng J, Wu C, Yang J (2001) Breeding of rice genic male sterile line SE21S and its utilization (in Chinese). Fujian Journal of Agricultural Sciences 16:1–4. https://doi.org/10.19303/j.issn.1008-0384.2001.03.001
Huang X, Feng Q, Qian Q, Zhao Q, Wang L, Wang A, Guan J, Fan D, Weng Q, Huang T, Dong G, Sang T, Han B (2009) High-throughput genotyping by whole-genome resequencing. Genome Res 19:1068–1076. https://doi.org/10.1101/gr.089516.108
Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967. https://doi.org/10.1038/ng.695
Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Lu Y, Weng Q, Han B (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633. https://doi.org/10.1038/nature19760
Huang X, Yang S, Gong J, Zhao Y, Feng Q, Gong H, Li W, Zhan Q, Cheng B, Xia J, Chen N, Hao Z, Liu K, Zhu C, Huang T, Zhao Q, Zhang L, Fan D, Zhou C, Lu Y, Weng Q, Wang ZX, Li J, Han B (2015) Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. Nat Commun 6:6258. https://doi.org/10.1038/ncomms7258
Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39. https://doi.org/10.1038/ng.1018
Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42:459–463. https://doi.org/10.1038/ng.550
Li S, Yang D, Zhu Y (2007) Characterization and use of male sterility in hybrid rice breeding. J Integr Plant Biol 49:791–804. https://doi.org/10.1111/j.1744-7909.2007.00513.x
Li X, Li XR, Fridman E, Tesso TT, Yu JM (2015) Dissecting repulsion linkage in the dwarfing gene Dw3 region for sorghum plant height provides insights into heterosis. P Natl Acad Sci USA 112:11823–11828. https://doi.org/10.1073/pnas.1509229112
Liu H, Deng Z, Deng L, Deng X (2012) Breeding and application of new strong heterosis hybrid rice combination Liangyou 1128 (in Chinese). Hybrid Rice 27:17–19,22. https://doi.org/10.16267/j.cnki.1005-3956.2012.04.008
Liu J, Li M, Zhang Q, Wei X, Huang X (2020) Exploring the molecular basis of heterosis for plant breeding. J Integr Plant Biol 62:287–298. https://doi.org/10.1111/jipb.12804
Luo D, Xu H, Liu Z, Guo J, Li H, Chen L, Fang C, Zhang Q, Bai M, Yao N, Wu H, Wu H, Ji C, Zheng H, Chen Y, Ye S, Li X, Zhao X, Li R, Liu YG (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577. https://doi.org/10.1038/ng.2570
Qin X, Wei S, Huang Y, Song Z (1994) Breeding and utilization of hybrid rice restorer line Gui 99 (in Chinese). Hybrid Rice 9:1–3
Tang H, Luo D, Zhou D, Zhang Q, Tian D, Zheng X, Chen L, Liu YG (2014) The rice restorer Rf4 for wild-abortive cytoplasmic male sterility encodes a mitochondrial-localized PPR protein that functions in reduction of WA352 transcripts. Mol Plant 7:1497–1500. https://doi.org/10.1093/mp/ssu047
Wang C, Tang S, Zhan Q, Hou Q, Zhao Y, Zhao Q, Feng Q, Zhou C, Lyu D, Cui L, Li Y, Miao J, Zhu C, Lu Y, Wang Y, Wang Z, Zhu J, Shangguan Y, Gong J, Yang S, Wang W, Zhang J, Xie H, Huang X, Han B (2019) Dissecting a heterotic gene through GradedPool-Seq mapping informs a rice-improvement strategy. Nat Commun 10:2982. https://doi.org/10.1038/s41467-019-11017-y
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
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 12:2473–2483. https://doi.org/10.1105/tpc.12.12.2473
Zhang B, Liu HY, Qi FX, Zhang ZY, Li QP, Han ZM, Xing YZ (2019a) Genetic interactions among Ghd7, Ghd8, OsPRR37 and Hd1 contribute to large variation in heading date in rice. Rice 12. https://doi.org/10.1186/s12284-019-0314-x
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. The New phytologist 208:1056–1066. https://doi.org/10.1111/nph.13538
Zhang ZY, Zhang B, Qi FX, Wu H, Li ZX, Xing YZ (2019b) 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 https://doi.org/10.1007/s11032-019-1001-8
Zhao Q, Feng Q, Lu H, Li Y, Wang A, Tian Q, Zhan Q, Lu Y, Zhang L, Huang T, Wang Y, Fan D, Zhao Y, Wang Z, Zhou C, Chen J, Zhu C, Li W, Weng Q, Xu Q, Wang ZX, Wei X, Han B, Huang X (2018) Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet 50:278–284. https://doi.org/10.1038/s41588-018-0041-z
Zhou G, Chen Y, Yao W, Zhang C, Xie W, Hua J, Xing Y, Xiao J, Zhang Q (2012) Genetic composition of yield heterosis in an elite rice hybrid. Proc Natl Acad Sci U S A 109:15847–15852. https://doi.org/10.1073/pnas.1214141109
Zhou H, Zhou M, Yang Y, Li J, Zhu L, Jiang D, Dong J, Liu Q, Gu L, Zhou L, Feng M, Qin P, Hu X, Song C, Shi J, Song X, Ni E, Wu X, Deng Q, Liu Z, Chen M, Liu YG, Cao X, Zhuang C (2014) RNase Z(S1) processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5:4884. https://doi.org/10.1038/ncomms5884
Zhou X, Huang X (2019) Genome-wide association studies in rice: how to solve the low power problems? Mol Plant 12:10–12. https://doi.org/10.1016/j.molp.2018.11.010
Funding
This work was supported by grants from the National Transgenic Science and Technology Program (2019ZX08010-003), Innovation Program of Shanghai Municipal Education Commission (2017-01-07-00-02-E00039), and Zhejiang Provincial Natural Science Foundation of China (LY18C130006).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liu, J., Gong, J., Wei, X. et al. Dominance complementation of Hd1 and Ghd8 contributes to extremely late flowering in two rice hybrids. Mol Breeding 40, 76 (2020). https://doi.org/10.1007/s11032-020-01162-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-020-01162-4