Abstract
Key message
Shuhui498 (R498) is an elite parent of heavy panicle hybrid rice by pyramiding the rare gn1a and null gs3 alleles. This finding reveals the genetic basis and great potential application in future breeding of R498.
Abstract
The heavy panicle trait, defined as 5 g or more of grain weight per panicle, is one of the target traits in super-high-yield rice breeding programs. The use of heavy panicle-type hybrid rice has been shown to be a successful strategy for super-high-yield breeding programs, particularly under the environmental conditions of high humidity and deficient solar radiation in southwestern China. However, the genetic components of the heavy panicle trait in hybrid rice remain elusive. Here, we report that the combination of loss-of-function mutations in Grain number 1a (Gn1a) and Grain Size 3 (GS3) is responsible for the heavy panicle phenotype of the elite hybrid rice restorer line Shuhui498 (R498). The null gn1a allele is the determinant factor for heavy panicles through increased grain number, while gs3 is associated with grain size and weight. R498 pyramided the two major null alleles, resulting in heavy panicles with a high grain number and large grains. Clustering analysis revealed that the null gn1aR498 allele is a rare haplotype which has been innovatively utilized in R498, underscoring the great potential of R498 for breeding purposes. Our research thus sheds light on the distinct genetic compositions of heavy panicle-type rice and may potentially facilitate super-high-yield rice breeding.
Similar content being viewed by others
References
Ashikari M et al (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745. https://doi.org/10.1126/science.1113373
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890
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
Danecek P et al (2011) The variant call format and VCF tools. Bioinformatics 27:2156–2158
Fan C et al (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
Fan C, Yu S, Wang C, Xing Y (2009) A causal C-A mutation in the second exon of GS3 highly associated with rice grain length and validated as a functional marker. Theor Appl Genet 118:465
Fujita D et al (2013) NAL1 allele from a rice landrace greatly increases yield in modern indica cultivars. Proc Natl Acad Sci USA 110:20431–20436. https://doi.org/10.1073/pnas.1310790110
Guo L-B, Ye G-Y (2014) Use of major quantitative trait loci to improve grain yield of rice. Rice Sci 21:65–82. https://doi.org/10.1016/s1672-6308(13)60174-2
He F, Xi Z, Zeng R, Talukdar A, Zhang G (2005) Mapping of heading date QTLs in rice (Oryza sativa L.) using single segment substitution lines. Sci Agric Sin 38:1505–1513
Huang Y (2001) Ecological breeding engineering for Chinese super rice characterized with seminar, early growth, deep roots, super high-yielding, and excellent quality. Guangdong Agric Sci 3:2–6
Huang X et al (2009a) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497. https://doi.org/10.1038/ng.352
Huang X et al (2009b) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497
Huang X et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501. https://doi.org/10.1038/nature11532
Huang X et al (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633. https://doi.org/10.1038/nature19760
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314
Ishimaru K et al (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45:707–711
Jianfeng et al (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209
Jiao Y et al (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544. https://doi.org/10.1038/ng.591
Jukes T, Cantor C (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York
Juliano BO, Villareal CP (1993) Grain quality evaluation of world rices. International Rice Research Institute, Manila
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Li D 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 USA 113:E6026–E6035. https://doi.org/10.1073/pnas.1610115113
Li S et al (2013) Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proc Natl Acad Sci USA 110:3167–3172. https://doi.org/10.1073/pnas.1300359110
Li H et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Li Y et al (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269
Luo D et al (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573
Ma G-H, Yuan L-P (2015) Hybrid rice achievements, development and prospect in China. J Integr Agric 14:197–205. https://doi.org/10.1016/s2095-3119(14)60922-9
Mao H et al (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc Natl Acad Sci USA 107:19579–19584
McKenna A et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
Mei F, Wu X, Yao C, Li L, Wang L, Chen Q (1988) Rice cropping regionalization in China. Chin J Rice Sci 2:97–110
Miura K et al (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549. https://doi.org/10.1038/ng.592
Miura K, Ashikari M, Matsuoka M (2011) The role of QTLs in the breeding of high-yielding rice. Trends Plant Sci 16:319–326
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420
Paterson AH, Deverna JW, Lanini B, Tanksley SD (1990) Fine mapping of quantitative trait loci using selected overlapping recombinant chromosomes, in an interspecies cross of tomato. Genetics 124:735
Peng S, Cassman KG, Virmani SS, Sheehy J, Khush GS (1999) Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Sci 39:1552–1559
Qi P et al (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22:1666–1680
Qian Q, Guo L, Smith SM, Li J (2016) Breeding high-yield superior quality hybrid super rice by rational design. Natl Sci Rev 3:283–294. https://doi.org/10.1093/nsr/nww006
Ramkumar G et al (2010) Development of a PCR-based SNP marker system for effective selection of kernel length and kernel elongation in rice. Mol Breed 26:735–740. https://doi.org/10.1007/s11032-010-9492-3
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shen L et al (2018) QTL editing confers opposing yield performance in different rice varieties. J Integr Plant Biol 60:89–93
Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630
Sun H et al (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656. https://doi.org/10.1038/ng.2958
Terao T, Nagata K, Morino K, Hirose T (2010) A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor Appl Genet 120:875–893
Tilman D et al (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284
Unnevehr LJ, Duff B, Juliano BO (1992) Consumer demand for rice grain quality. International Rice Research Institute, Manila
Wang E et al (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374
Wang S et al (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954
Wang J, Xu H, Li N, Fan F, Wang L, Zhu Y, Li S (2015) Artificial selection of Gn1a plays an important role in improving rice yields across different ecological regions. Rice (N Y) 8:37. https://doi.org/10.1186/s12284-015-0071-4
Wei X et al (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758. https://doi.org/10.1104/pp.110.156943
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Wu Y, Bhat PR, Close TJ, Lonardi S (2008) Efficient and accurate construction of genetic linkage maps from the minimum spanning tree of a graph. PLoS Genet 4:e1000212
Wu Y, Wang Y, Mi XF, Shan JX, Li XM, Xu JL, Lin HX (2016) The QTL GNP1 encodes GA20ox1, which increases grain number and yield by increasing cytokinin activity in rice panicle meristems. PLoS Genet 12:e1006386. https://doi.org/10.1371/journal.pgen.1006386
Xu Y (2003) Developing marker-assisted selection strategies for breeding hybrid rice. Plant Breed Rev 23:73–174
Xu H, Zhao M, Zhang Q, Xu Z, Xu Q (2016) The DENSE AND ERECT PANICLE 1 (DEP1) gene offering the potential in the breeding of high-yielding rice. Breed Sci 66:659–667. https://doi.org/10.1270/jsbbs.16120
Xue W et al (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
Yang S (1984) The theory and method of ideal plant morphology in rice breeding. Sci Agric Sin 3:6–13
Yuan L (1997) Hybrid rice breeding for super high yield. Hybrid Rice 27:1–6
Zhang GH 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. https://doi.org/10.1093/mp/ssu055
Zheng T et al (2015) Rice functional genomics and breeding database (RFGB)-3K-rice SNP and InDel sub-database. Chin J 60:367
Zhou K (1997) The study on heavy panicle type of inter subspecific hybrid rice (Oryza sativa L). Sci Agric Sin 30:91–93
Zhou K, Ma Y, Liu T, Shen M (1995) The breeding of subspecific heavy ear hybrid rice exploration about super-high yield breeding of hybrid rice. J Sichuan Agric Univ 13:403–407
Zhou L-J, Jiang L, Zhai H-Q, Wan J-M (2009) Current status and strategies for improvement of rice grain chalkiness. Hereditas (Beijing) 31:563–572. https://doi.org/10.3724/sp.j.1005.2009.00563
Zhou G et al (2012) Genetic composition of yield heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 109:15847–15852. https://doi.org/10.1073/pnas.1214141109
Zuo J, Li J (2014) Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu Rev Genet 48:99–118. https://doi.org/10.1146/annurev-genet-120213-092138
Acknowledgements
We thank Prof. Dengcai Liu, Prof. Wenming Wang, and Prof. Xuewei Chen of SCAU (Sichuan Agricultural University) for editing and providing comments regarding this manuscript. This research was supported by Grant NSFC 91735304 and 31571441 from the National Science Foundation of China, Breeding New Cultivar of Super Green Rice (2014AA10A604), State Key Laboratory of Hybrid Rice (2016KF09) and Key Research Project of Sichuan Provincial Education Department (14ZA0013).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing financial interests.
Additional information
Communicated by Takuji Sasaki.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, S., Ma, B., Gao, Q. et al. Dissecting the genetic basis of heavy panicle hybrid rice uncovered Gn1a and GS3 as key genes. Theor Appl Genet 131, 1391–1403 (2018). https://doi.org/10.1007/s00122-018-3085-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-018-3085-7