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Volume 49 Issue 5
May  2022
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Article Contents

Fixation of hybrid sterility genes and favorable alleles of key yield-related genes with dominance contribute to the high yield of the Yongyou series of intersubspecific hybrid rice

doi: 10.1016/j.jgg.2022.02.027
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The computations in this article were run on the bioinformatics computing platform of the National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University. This work was partially supported by funds from the National Natural Science Foundation of China (32061143042, 31821005, 91935302) and The National Key Research and Development Program of China (2016YFD0100802).

  • Received Date: 2021-12-31
  • Accepted Date: 2022-02-20
  • Rev Recd Date: 2022-02-12
  • Publish Date: 2022-03-16
  • In rice, the Yongyou series of Xian-Geng intersubspecific hybrids have excellent production performance, as shown by their extremely high yield. However, the mechanisms underlying the success of these rice hybrids are unclear. In this study, three F2 populations are generated from three Yongyou hybrids to determine the genetic basis of the extremely high yield of intersubspecific hybrids. Genome constitution analysis reveals that the female and male parental lines belong to the Geng and Xian subspecies, respectively, although introgression of 20% of the Xian ancestry and 14% of the Geng ancestry are observed. Twenty-five percent of the hybrid genomes carries homozygous Xian or Geng fragments, which harbors hybrid sterility genes such as Sd, Sc, f5, and qS12 and favorable alleles of key yield-related genes, including NAL1, Ghd7, and Ghd8. None of the parents carries the S5+ killer of the S5 killer-protector system. Compatible allele combinations of hybrid sterility genes ensure the fertility of these intersubspecific hybrids and overcome the bottleneck in applying intersubspecific hybrids. Additive effects of favorable alleles of yield-related genes fixed in both parents enhances midparent values. Many QTLs for yield and its key component spikelets per panicle shows dominance and the net positive dominant effects lead to heterosis. These factors result in an extremely high yield of the hybrids. These findings will aid in the development of new intersubspecific rice hybrids with diverse genetic backgrounds.
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  • Alexander, D.H., Novembre, J.,Lange, K., 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664
    Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano, H.,Matsuoka, M., 2005. Cytokinin oxidase regulates rice grain production. Science 309, 741-745
    Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y.,Buckler, E.S., 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633-2635
    Bruce, A.B., 1910. The Mendelian Theory of Heredity and the Augmentation of Vigor. Science 32, 627-628
    Chang, C.C., Chow, C.C., Tellier, L.C., Vattikuti, S., Purcell, S.M.,Lee, J.J., 2015. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4, 7
    Chen, L.,Liu, Y.G., 2014. Male sterility and fertility restoration in crops. Annu. Rev. Plant Biol. 65, 579-606
    Danecek, P., Bonfield, J.K., Liddle, J., Marshall, J., Ohan, V., Pollard, M.O., Whitwham, A., Keane, T., McCarthy, S.A., Davies, R.M., et al., 2021. Twelve years of SAMtools and BCFtools. Gigascience 10
    East, E.M., 1908. Inbreeding in corn. Rep. Conn. Agric. Exp. Stn. 1907, 419-428
    Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S.,Mitchell, S.E., 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379
    Fan, C., Xing, Y., Mao, H., Lu, T., Han, B., Xu, C., Li, X.,Zhang, Q., 2006. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164-1171
    Gonda, I., Ashrafi, H., Lyon, D.A., Strickler, S.R., Hulse-Kemp, A.M., Ma, Q., Sun, H., Stoffel, K., Powell, A.F., Futrell, S., et al., 2019. Sequencing-Based Bin Map Construction of a Tomato Mapping Population, Facilitating High-Resolution Quantitative Trait Loci Detection. Plant Genome 12, 180010
    Hu, Z.J., Lu, S.J., Wang, M.J., He, H.H., Sun, L., Wang, H.R., Liu, X.H., Jiang, L., Sun, J.L., Xin, X.Y., et al., 2018. A Novel QTL qTGW3 Encodes the GSK3/SHAGGY-Like Kinase OsGSK5/OsSK41 that Interacts with OsARF4 to Negatively Regulate Grain Size and Weight in Rice. Mol. Plant 11, 736-749
    Hua, J., Xing, Y., Wu, W., Xu, C., Sun, X., Yu, S.,Zhang, Q., 2003. Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. U. S. A. 100, 2574-2579
    Huang, X., Yang, S., Gong, J., Zhao, Q., Feng, Q., Zhan, Q., Zhao, Y., Li, W., Cheng, B., Xia, J., et al., 2016. Genomic architecture of heterosis for yield traits in rice. Nature 537, 629-633
    Huang, X., Yang, S., Gong, J., Zhao, Y., Feng, Q., Gong, H., Li, W., Zhan, Q., Cheng, B., Xia, J., et al., 2015. Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. Nat. Commun. 6, 6258
    Huo, X., Wu, S., Zhu, Z., Liu, F., Fu, Y., Cai, H., Sun, X., Gu, P., Xie, D., Tan, L., et al., 2017. NOG1 increases grain production in rice. Nat. Commun. 8, 1497
    Jakobsson, M.,Rosenberg, N.A., 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801-1806
    Jones, D.F., 1917. Dominance of linked factors as a means of accounting for heterosis. Genetics 2, 466
    Kosambi, D.D., 1943. The estimation of map distances from recombination values. Ann. Eugen. 12, 172-175
    Krieger, U., Lippman, Z.B.,Zamir, D., 2010. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42, 459-463
    Li, D., Huang, Z., Song, S., Xin, Y., Mao, D., Lv, Q., Zhou, M., Tian, D., Tang, M., Wu, Q., et al., 2016. Integrated analysis of phenome, genome, and transcriptome of hybrid rice uncovered multiple heterosis-related loci for yield increase. Proc. Natl. Acad. Sci. U. S. A. 113, E6026-E6035
    Li, H.,Durbin, R., 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760
    Li, M.X., Yeung, J.M., Cherny, S.S.,Sham, P.C., 2012. Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum. Genet. 131, 747-756
    Li, W., Zeng, R., Zhang, Z., Ding, X.,Zhang, G., 2008. Identification and fine mapping of S-d, a new locus conferring the partial pollen sterility of intersubspecific F1 hybrids in rice (Oryza sativa L.). Theor. Appl. Genet. 116, 915-922
    Li, X., Chen, Z., Zhang, G., Lu, H., Qin, P., Qi, M., Yu, Y., Jiao, B., Zhao, X., Gao, Q., et al., 2020. Analysis of genetic architecture and favorable allele usage of agronomic traits in a large collection of Chinese rice accessions. Sci. China Life Sci. 63, 1688-1702
    Liang, Q.Z., Shang, L.G., Wang, Y.M.,Hua, J.P., 2015. Partial Dominance, Overdominance and Epistasis as the Genetic Basis of Heterosis in Upland Cotton (Gossypium hirsutum L.). PLoS One 10, e0143548
    Lin, T., Zhou, C., Chen, G., Yu, J., Wu, W., Ge, Y., Liu, X., Li, J., Jiang, X., Tang, W., et al., 2020a. Heterosis-associated genes confer high yield in super hybrid rice. Theor. Appl. Genet. 133, 3287-3297
    Lin, Z., Qin, P., Zhang, X., Fu, C., Deng, H., Fu, X., Huang, Z., Jiang, S., Li, C., Tang, X., et al., 2020b. Divergent selection and genetic introgression shape the genome landscape of heterosis in hybrid rice. Proc. Natl. Acad. Sci. U. S. A. 117, 4623-4631
    Lv, C.,Zou, J.-s., 2016. Theory and practice on breeding of two-line hybrid rice, Liangyoupeijiu. Scientia Agricultura Sinica 49, 1635-1645
    Lv, Q., Li, W., Sun, Z., Ouyang, N., Jing, X., He, Q., Wu, J., Zheng, J., Zheng, J., Tang, S., et al., 2020. Resequencing of 1,143 indica rice accessions reveals important genetic variations and different heterosis patterns. Nat. Commun. 11, 4778
    Ma, R., Wang, X., Lu, Y., Zhou, H., Cai, K., Li, X.,Zhang, Z., 2010. Breeding and application of late japonica CMS line Yongjing 2A and its late indica-japonica hybrid rice Combinations. Zajiao Shuidao 25, 185-189
    McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al., 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303
    Meng, L., Li, H.H., Zhang, L.Y.,Wang, J.K., 2015. QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J. 3, 269-283
    Mi, J., Li, G., Huang, J., Yu, H., Zhou, F., Zhang, Q., Ouyang, Y.,Mou, T., 2016. Stacking S5-n and f5-n to overcome sterility in indica-japonica hybrid rice. Theor. Appl. Genet. 129, 563-575
    Mi, J.M., Lei, Y., Kim, S.R., Prahalada, G.D., Ouyang, Y.D.,Mou, T.M., 2019. An effective strategy for fertility improvement of indica-japonica hybrid rice by pyramiding S5-n, f5-n, and pf12-j. Mol. Breed. 39, 138
    Minvielle, F., 1987. Dominance Is Not Necessary for Heterosis: a two-Locus Model. Genet. Res. 49, 245-247
    Moll, R.H., Salhuana, W.,Robinson, H., 1962. Heterosis and genetic diversity in variety crosses of maize. Crop Sci. 2, 197-198
    Ouyang, Y., 2016. Progress of indica-japonica hybrid sterility and wide-compatibility in rice. Chin. Sci. Bull. 61, 3833-3841
    Ouyang, Y., Li, G., Mi, J., Xu, C., Du, H., Zhang, C., Xie, W., Li, X., Xiao, J., Song, H., et al., 2016. Origination and Establishment of a Trigenic Reproductive Isolation System in Rice. Mol. Plant 9, 1542-1545
    Schliep, K.P., 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592-593
    Schnell, F.W.,Cockerham, C.C., 1992. Multiplicative vs. arbitrary gene action in heterosis. Genetics 131, 461-469
    Shen, R., Wang, L., Liu, X., Wu, J., Jin, W., Zhao, X., Xie, X., Zhu, Q., Tang, H., Li, Q., et al., 2017. Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice. Nat. Commun. 8, 1310
    Shen, X., Chen, S.,Cao, L., 2008. Construction of genetic linkage map based on a RIL population derived from super hybrid rice, XY9308. Molecular Plant Breeding
    Shull, G.H., 1908. The composition of a field of maize. J. Hered., 296-301
    Song, X., Lin, J.,Wu, M., 2016. Review and prospect on utilization of heterosis between indica-japonica rice subspecies. Chin. Sci. Bull. 61, 3778-3786
    Song, X.J., Huang, W., Shi, M., Zhu, M.Z.,Lin, H.X., 2007. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623-630
    Stuber, C.W., Lincoln, S.E., Wolff, D., Helentjaris, T.,Lander, E., 1992. Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132, 823-839
    Tan, X.L., Tan, Y.L., Zhao, Y.H., Zhang, X.M., Hong, R.K., Jin, S.L., Liu, X.R.,Huang, D.J., 2004. Identification of the Rf gene conferring fertility restoration of the CMS Dian-type 1 in rice by using simple sequence repeat markers and advanced inbred lines of restorer and maintainer. Plant Breed. 123, 338-341
    Taylor, J.,Butler, D., 2017. R Package ASMap: Efficient Genetic Linkage Map Construction and Diagnosis. J. Stat. Softw. 79, 1-29
    Ting, Y., 1949. Origination of the rice cultivation in China. J. College of Agric. Sun Yat-Sen University 7, 11-24
    Wang, G.W., He, Y.Q., Xu, C.G.,Zhang, Q., 2006. Fine mapping of f5-Du, a gene conferring wide-compatibility for pollen fertility in inter-subspecific hybrids of rice (Oryza sativa L.). Theor. Appl. Genet. 112, 382-387
    Wang, W., Mauleon, R., Hu, Z., Chebotarov, D., Tai, S., Wu, Z., Li, M., Zheng, T., Fuentes, R.R., Zhang, F., et al., 2018. Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557, 43-49
    Wang, Y.X., Xiong, G.S., Hu, J., Jiang, L., Yu, H., Xu, J., Fang, Y.X., Zeng, L.J., Xu, E.B., Xu, J., et al., 2015. Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat. Genet. 47, 944-+
    Wei, H., Jiang, Y., Zhao, K., Xu, J., Zhang, H., Huo, Z., Xu, K., Wei, H., Zheng, F.,others, 2013. Characteristics of super-high yield population in Yongyou series of hybrid rice. Acta Agronomica Sinica 39, 2201-2210
    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., et al., 2013. Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc. Natl. Acad. Sci. U. S. A. 110, 2775-2780
    Xiao, J.H., Li, J.M., Yuan, L.P.,Tanksley, S.D., 1995. Dominance Is the Major Genetic-Basis of Heterosis in Rice as Revealed by Qtl Analysis Using Molecular Markers. Genetics 140, 745-754
    Xie, W., Wang, G., Yuan, M., Yao, W., Lyu, K., Zhao, H., Yang, M., Li, P., Zhang, X., Yuan, J., et al., 2015. Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection. Proc. Natl. Acad. Sci. U. S. A. 112, E5411-5419
    Xie, Y., Shen, R., Chen, L.,Liu, Y.G., 2019. Molecular mechanisms of hybrid sterility in rice. Sci. China Life Sci. 62, 737-743
    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., et al., 2011. A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol. Plant 4, 319-330
    Yang, J.Y., Zhao, X.B., Cheng, K., Du, H.Y., Ouyang, Y.D., Chen, J.J., Qiu, S.Q., Huang, J.Y., Jiang, Y.H., Jiang, L.W., et al., 2012. A Killer-Protector System Regulates Both Hybrid Sterility and Segregation Distortion in Rice. Science 337, 1336-1340
    Yano, K., Morinaka, Y., Wang, F., Huang, P., Takehara, S., Hirai, T., Ito, A., Koketsu, E., Kawamura, M., Kotake, K., et al., 2019. GWAS with principal component analysis identifies a gene comprehensively controlling rice architecture. Proc. Natl. Acad. Sci. U. S. A. 116, 21262-21267
    Yano, K., Ookawa, T., Aya, K., Ochiai, Y., Hirasawa, T., Ebitani, T., Takarada, T., Yano, M., Yamamoto, T., Fukuoka, S., et al., 2015. Isolation of a novel lodging resistance QTL gene involved in strigolactone signaling and its pyramiding with a QTL gene involved in another mechanism. Mol. Plant 8, 303-314
    Yu, B., Lin, Z., Li, H., Li, X., Li, J., Wang, Y., Zhang, X., Zhu, Z., Zhai, W., Wang, X., et al., 2007. TAC1, a major quantitative trait locus controlling tiller angle in rice. Plant J. 52, 891-898
    Yu, G.C., Smith, D.K., Zhu, H.C., Guan, Y.,Lam, T.T.Y., 2017. GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28-36
    Yu, S.B., Li, J.X., Xu, C.G., Tan, Y.F., Gao, Y.J., Li, X.H., Zhang, Q.,Saghai Maroof, M.A., 1997. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. U. S. A. 94, 9226-9231
    Yu, Y., Hu, X., Zhu, Y.,Mao, D., 2020. Re-evaluation of the rice ‘Green Revolution’ gene: the weak allele SD1-EQ from japonica rice may be beneficial for super indica rice breeding in the post-Green Revolution era. Mol. Breed. 40, 84
    Zhang, B., Liu, H.Y., Qi, F.X., Zhang, Z.Y., Li, Q.P., Han, Z.M.,Xing, Y.Z., 2019. Genetic Interactions Among Ghd7, Ghd8, OsPRR37 and Hd1 Contribute to Large Variation in Heading Date in Rice. Rice 12, 1-13
    Zhang, G.H., Li, S.Y., Wang, L., Ye, W.J., Zeng, D.L., Rao, Y.C., Peng, Y.L., Hu, J., Yang, Y.L., Xu, J., et al., 2014. LSCHL4 from Japonica Cultivar, which is allelic to NAL1, increases yield of indica super rice 93-11. Mol. Plant 7, 1350-1364
    Zhang, H., Zhang, C.Q., Sun, Z.Z., Yu, W., Gu, M.H., Liu, Q.Q.,Li, Y.S., 2011. A major locus qS12, located in a duplicated segment of chromosome 12, causes spikelet sterility in an indica-japonica rice hybrid. Theor. Appl. Genet. 123, 1247-1256
    Zhang, J., Zhou, X., Yan, W., Zhang, Z., Lu, L., Han, Z., Zhao, H., Liu, H., Song, P., Hu, Y., et al., 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, C., Sun, Y., Wang, D., Sun, W., Yu, Y., Hu, Z.,Yu, S., 2021. Dissection of heterotic loci for grain yield using interconnected chromosome segment substitution lines in rice. Crop J
    Zhang, L., Yu, H., Ma, B., Liu, G., Wang, J., Wang, J., Gao, R., Li, J., Liu, J., Xu, J., et al., 2017. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat. Commun. 8, 14789
    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
    Zhou, X., Nong, C., Wu, B., Zhou, T., Zhang, B., Liu, X., Gao, G., Mi, J., Zhang, Q., Liu, H., et al., 2021. Combinations of Ghd7, Ghd8, and Hd1 determine strong heterosis of commercial rice hybrids in diverse ecological regions. J. Exp. Bot. 72, 6963-6976
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