Abstract
The key to food security is increasing rice yield. Therefore, we performed a genome-wide association study (GWAS) to analyse and identify the effects of plant height (PH), effective tiller number (ETN), heading date (HD) and grain weight per plant (GWPP) on rice yield using 1,220,522 single-nucleotide polymorphisms (SNPs) from 168 rice accessions. The PH, ETN, HD, and GWPP phenotypes of the 168 rice accessions were analysed in 2019, 2020 and 2021, and an abundance of phenotypic variation was found. One QTL for PH was detected on chromosome 4, one QTL for ETN on chromosome 11, two QTLs for GWPP on chromosome 2, and one QTL for HD on chromosome 5, all of which were detected in 3 years of the study period through a general linear model (GLM) and mixed linear model (MLM). We detected two QTLs related to the traits by using multi-trait GWAS. In addition, we identified four novel genes responsible for rice yield. Haplotype analysis indicated that LOC_Os02g07680 was highly associated with GWPP, LOC_Os11g18570 was highly associated with ETN, LOC_Os04g49210 was highly associated with HD, and LOC_Os05g34600 was highly associated with PH. The results provide important genetic information for PH, ETN, HD and GWPP studies, laying the foundation for increasing rice yield.
Similar content being viewed by others
Abbreviations
- GWAS:
-
Genome-wide association study
- LD:
-
Linkage disequilibrium
- PCA:
-
Principal component analysis
- GLM:
-
General linear model
- MLM:
-
Mixed linear model
- CV:
-
Coefficient of variation
- HB 2 :
-
Broad-sense heritability
- PVE:
-
Phenotypic variation explained
- SNP:
-
Single nucleotide polymorphism
- QTL:
-
Quantitative trait locus
- HD:
-
Heading date
- PH:
-
Plant height
- ETN:
-
Effective tiller number
- GWPP:
-
Grain weight per plant
References
Barnett GC, Thompson D, Fachal L, Kerns S, Talbot C, Elliott RM, Dorling L, Coles CE, Dearnaley DP, Rosenstein BS, Vega A, Symonds P, Yarnold J, Baynes C, Michailidou K, Dennis J, Tyrer JP, Wilkinson JS, Gomez-Caamano A, Tanteles GA, Platte R, Mayes R, Conroy D, Maranian M, Luccarini C, Gulliford SL, Sydes MR, Hall E, Haviland J, Misra V, Titley J, Bentzen SM, Pharoah PD, Burnet NG, Dunning AM, West CM (2014) A genome wide association study (GWAS) providing evidence of an association between common genetic variants and late radiotherapy toxicity. Radiother Oncol 111(2):178–185. https://doi.org/10.1016/j.radonc.2014.02.012
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300
Borna RS, Murchie EH, Pyke KA, Roberts JA, Gonzalez-Carranza ZH (2022) The rice EP3 and OsFBK1 E3 ligases alter plant architecture and flower development, and affect transcript accumulation of microRNA pathway genes and their targets. Plant Biotechnol J 20(2):297–309. https://doi.org/10.1111/pbi.13710
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Cai L-J, Yun H, Zhong X-L, Du D, Peng X-M, Dai J-C, Yang Z-L, Zhao F-M, Zhang C-W (2021a) Identification and QTL mapping of important agronomic traits based on rice short-wide grain CSSL-Z752 with restorer line Xihui 18 as background. Cereal Res Commun 50(3):473–480. https://doi.org/10.1007/s42976-021-00195-5
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 (2021b) DHD4, a CONSTANS-like family transcription factor, delays heading date by affecting the formation of the FAC complex in rice. Mol Plant 14(2):330–343. https://doi.org/10.1016/j.molp.2020.11.013
Chaban C, Waller F, Furuya M, Nick P (2003) Auxin responsiveness of a novel cytochrome p450 in rice coleoptiles. Plant Physiol 133(4):2000–2009. https://doi.org/10.1104/pp.103.022202
Chai J, Zhu S, Li C, Wang C, Cai M, Zheng X, Zhou L, Zhang H, Sheng P, Wu M, Jin X, Cheng Z, Zhang X, Lei C, Ren Y, Lin Q, Zhou S, Guo X, Wang J, Zhao Z, Wan J (2021) OsRE1 interacts with OsRIP1 to regulate rice heading date by finely modulating Ehd1 expression. Plant Biotechnol J 19(2):300–310. https://doi.org/10.1111/pbi.13462
Chen W, Cheng Z, Liu L, Wang M, You X, Wang J, Zhang F, Zhou C, Zhang Z, Zhang H, You S, Wang Y, Luo S, Zhang J, Wang J, Wang J, Zhao Z, Guo X, Lei C, Zhang X, Lin Q, Ren Y, Zhu S, Wan J (2019) Small grain and Dwarf 2, encoding an HD-Zip II family transcription factor, regulates plant development by modulating gibberellin biosynthesis in rice. Plant Sci 288:110208. https://doi.org/10.1016/j.plantsci.2019.110208
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(8):926–936. https://doi.org/10.1101/gad.1189604
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Gao H, Jin M, Zheng XM, 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 U S A 111(46):16337–16342. https://doi.org/10.1073/pnas.1418204111
Gu H, Zhang K, Chen J, Gull S, Chen C, Hou Y, Li X, Miao J, Zhou Y, Liang G (2022) OsFTL4, an FT-like gene, regulates flowering time and drought tolerance in rice (Oryza sativa L.). Rice (n y) 15(1):47. https://doi.org/10.1186/s12284-022-00593-1
Guo S, Xu Y, Liu H, Mao Z, Zhang C, Ma Y, Zhang Q, Meng Z, Chong K (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4:1566. https://doi.org/10.1038/ncomms2542
Guo M, Yang Y-H, Liu M, Meng Q-C, Zeng X-H, Dong L-X, Tang S-Z, Gu M-H, Yan C-J (2014) Clustered spikelets 4, encoding a putative cytochrome P450 protein CYP724B1, is essential for rice panicle development. Chin Sci Bull 59(31):4050–4059. https://doi.org/10.1007/s11434-014-0568-z
Hirano K, Yoshida H, Aya K, Kawamura M, Hayashi M, Hobo T, Sato-Izawa K, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2017) Small organ size 1 and small organ size 2/Dwarf and low-tillering form a complex to integrate auxin and brassinosteroid signaling in rice. Mol Plant 10(4):590–604. https://doi.org/10.1016/j.molp.2016.12.013
Hofer R, Boachon B, Renault H, Gavira C, Miesch L, Iglesias J, Ginglinger JF, Allouche L, Miesch M, Grec S, Larbat R, Werck-Reichhart D (2014) Dual function of the cytochrome P450 CYP76 family from Arabidopsis thaliana in the metabolism of monoterpenols and phenylurea herbicides. Plant Physiol 166(3):1149–1161. https://doi.org/10.1104/pp.114.244814
Hou M, Luo F, Wu D, Zhang X, Lou M, Shen D, Yan M, Mao C, Fan X, Xu G, Zhang Y (2021) OsPIN9, an auxin efflux carrier, is required for the regulation of rice tiller bud outgrowth by ammonium. New Phytol 229(2):935–949. https://doi.org/10.1111/nph.16901
Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B, Onishi A, Miyagawa H, Katoh E (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45(6):707–711. https://doi.org/10.1038/ng.2612
Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, Yi W, Zhao L, Ma H, He Y, Wu Z, Melcher K, Qian Q, Xu HE, Wang Y, Li J (2013) Dwarf 53 acts as a repressor of strigolactone signalling in rice. Nature 504(7480):401–405. https://doi.org/10.1038/nature12870
Jung C, Muller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14(10):563–573. https://doi.org/10.1016/j.tplants.2009.07.005
Jung H, Lee DK, Choi YD, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312. https://doi.org/10.1016/j.plantsci.2015.04.018
Kadambari G, Vemireddy LR, Srividhya A, Nagireddy R, Jena SS, Gandikota M, Patil S, Veeraghattapu R, Deborah DAK, Reddy GE, Shake M, Dasari A, Ramanarao PV, Durgarani CV, Neeraja CN, Siddiq EA, Sheshumadhav M (2018) QTL-Seq-based genetic analysis identifies a major genomic region governing dwarfness in rice (Oryza sativa L.). Plant Cell Rep 37(4):677–687. https://doi.org/10.1007/s00299-018-2260-2
Koumoto T, Shimada H, Kusano H, She K-C, Iwamoto M, Takano M (2013) Rice monoculm mutation moc2, which inhibits outgrowth of the second tillers, is ascribed to lack of a fructose-1,6-bisphosphatase. Plant Biotechnol 30(1):47–56. https://doi.org/10.5511/plantbiotechnology.12.1210a
Lee S, Jia MH, Jia Y, Liu G (2014) Tagging quantitative trait loci for heading date and plant height in important breeding parents of rice (Oryza sativa). Euphytica 197(2):191–200. https://doi.org/10.1007/s10681-013-1051-7
Li ZK, Yu SB, Lafitte HR, Huang N, Courtois B, Hittalmani S, Vijayakumar CH, Liu GF, Wang GC, Shashidhar HE, Zhuang JY, Zheng KL, Singh VP, Sidhu JS, Srivantaneeyakul S, Khush GS (2003) QTL x environment interactions in rice. I. Heading date and plant height. Theor Appl Genet 108(1):141–153. https://doi.org/10.1007/s00122-003-1401-2
Li M, Tang D, Wang K, Wu X, Lu L, Yu H, Gu M-h, Yan C, Cheng ZJ (2011) Mutations in the F-box gene larger panicle improve the panicle architecture and enhance the grain yield in rice. Plant Biotechnol J 9(9):1002–1013
Li X, Shi S, Tao Q, Tao Y, Miao J, Peng X, Li C, Yang Z, Zhou Y, Liang G (2019) OsGASR9 positively regulates grain size and yield in rice (Oryza sativa). Plant Sci 286:17–27. https://doi.org/10.1016/j.plantsci.2019.03.008
Li Z, Wei X, Tong X, Zhao J, Liu X, Wang H, Tang L, Shu Y, Li G, Wang Y, Ying J, Jiao G, Hu H, Hu P, Zhang J (2022) The OsNAC23-Tre6P-SnRK1a feed-forward loop regulates sugar homeostasis and grain yield in rice. Mol Plant 15(4):706–722. https://doi.org/10.1016/j.molp.2022.01.016
Liang WH, Shang F, Lin QT, Lou C, Zhang J (2014) Tillering and panicle branching genes in rice. Gene 537(1):1–5. https://doi.org/10.1016/j.gene.2013.11.058
Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang JL, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J (2012) Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1. Nat Commun 3:752. https://doi.org/10.1038/ncomms1716
Lin Q, Zhang Z, Wu F, Feng M, Sun Y, Chen W, Cheng Z, Zhang X, Ren Y, Lei C, Zhu S, Wang J, Zhao Z, Guo X, Wang H, Wan J (2020) The APC/C(TE) E3 ubiquitin ligase complex mediates the antagonistic regulation of root growth and tillering by ABA and GA. Plant Cell 32(6):1973–1987. https://doi.org/10.1105/tpc.20.00101
Liu X, Liu H, Zhang Y, He M, Li R, Meng W, Wang Z, Li X, Bu Q (2021) Fine-tuning flowering time via genome editing of upstream open reading frames of heading date 2 in rice. Rice (n y) 14(1):59. https://doi.org/10.1186/s12284-021-00504-w
Lu G, Coneva V, Casaretto JA, Ying S, Mahmood K, Liu F, Nambara E, Bi YM, Rothstein SJ (2015) OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. Plant J 83(5):913–925. https://doi.org/10.1111/tpj.12939
Luo A, Qian Q, Yin H, Liu X, Yin C, Lan Y, Tang J, Tang Z, Cao S, Wang X, Xia K, Fu X, Luo D, Chu C (2006) EUI1, encoding a putative cytochrome P450 monooxygenase, regulates internode elongation by modulating gibberellin responses in rice. Plant Cell Physiol 47(2):181–191. https://doi.org/10.1093/pcp/pci233
Magome H, Nomura T, Hanada A, Takeda-Kamiya N, Ohnishi T, Shinma Y, Katsumata T, Kawaide H, Kamiya Y, Yamaguchi S (2013) CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc Natl Acad Sci U S A 110(5):1947–1952. https://doi.org/10.1073/pnas.1215788110
Mongiano G, Titone P, Pagnoncelli S, Sacco D, Tamborini L, Pilu R, Bregaglio S (2020) Phenotypic variability in Italian rice germplasm. Eur J Agron 120. https://doi.org/10.1016/j.eja.2020.126131
Morales KY, Singh N, Perez FA, Ignacio JC, Thapa R, Arbelaez JD, Tabien RE, Famoso A, Wang DR, Septiningsih EM, Shi Y, Kretzschmar T, McCouch SR, Thomson MJ (2020) An improved 7K SNP array, the C7AIR, provides a wealth of validated SNP markers for rice breeding and genetics studies. PLoS ONE 15(5):e0232479. https://doi.org/10.1371/journal.pone.0232479
Nagai K, Mori Y, Ishikawa S, Furuta T, Gamuyao R, Niimi Y, Hobo T, Fukuda M, Kojima M, Takebayashi Y, Fukushima A, Himuro Y, Kobayashi M, Ackley W, Hisano H, Sato K, Yoshida A, Wu J, Sakakibara H, Sato Y, Tsuji H, Akagi T, Ashikari M (2020) Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature 584(7819):109–114. https://doi.org/10.1038/s41586-020-2501-8
Naruoka Y, Talbert LE, Lanning SP, Blake NK, Martin JM, Sherman JD (2011) Identification of quantitative trait loci for productive tiller number and its relationship to agronomic traits in spring wheat. Theor Appl Genet 123(6):1043–1053. https://doi.org/10.1007/s00122-011-1646-0
Piao HL, Xuan YH, Park SH, Je BI, Park SJ, Park SH, Kim CM, Huang J, Wang GK, Kim MJ, Kang SM, Lee IJ, Kwon TR, Kim YH, Yeo US, Yi G, Son D, Han CD (2010) OsCIPK31, a CBL-interacting protein kinase is involved in germination and seedling growth under abiotic stress conditions in rice plants. Mol Cells 30(1):19–27. https://doi.org/10.1007/s10059-010-0084-1
Pinot F, Beisson F (2011) Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles. FEBS J 278(2):195–205. https://doi.org/10.1111/j.1742-4658.2010.07948.x
Porter HF, O’Reilly PF (2017) Multivariate simulation framework reveals performance of multi-trait GWAS methods. Sci Rep. https://doi.org/10.1038/srep38837
Pritchard JK, Rosenberg NA (1999) Use of unlinked genetic markers to detect population stratification in association studies. Am J Hum Genet 65(1):220–228. https://doi.org/10.1086/302449
Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67(1):170–181. https://doi.org/10.1086/302959
Qiao F, Zhao K-J (2011) The influence of RNAi targeting of OsGA20ox2 gene on plant height in rice. Plant Mol Biol Report 29(4):952–960. https://doi.org/10.1007/s11105-011-0309-2
Ruan B, Shang L, Zhang B, Hu J, Wang Y, Lin H, Zhang A, Liu C, Peng Y, Zhu L, Ren D, Shen L, Dong G, Zhang G, Zeng D, Guo L, Qian Q, Gao Z (2020) Natural variation in the promoter ofTGW2determines grain width and weight in rice. New Phytol 227(2):629–640. https://doi.org/10.1111/nph.16540
Seck PA, Diagne A, Mohanty S, Wopereis MCS (2012) Crops that feed the world 7: rice. Food Secur 4(1):7–24. https://doi.org/10.1007/s12571-012-0168-1
Sharma P, Kumar V, Khosla R, Guleria P (2020) Exogenous naringenin improved digestible protein accumulation and altered morphology via VrPIN and auxin redistribution in Vigna radiata. 3 Biotech 10(10):431. https://doi.org/10.1007/s13205-020-02428-6
Shearman JR, Vejchasarn P, Naktang C, Phansenee Y, Jomchai N, Lanceras-Siangliw J, Tangphatsornruang S, Toojinda T (2022) Rice height QTLs in KDML105 chromosome segment substitution lines. Genomics 114(1):482–487. https://doi.org/10.1016/j.ygeno.2019.09.003
Shi Z, Rao Y, Xu J, Hu S, Fang Y, Yu H, Pan J, Liu R, Ren D, Wang X, Zhu Y, Zhu L, Dong G, Zhang G, Zeng D, Guo L, Hu J, Qian Q (2015) Characterization and cloning of SMALL GRAIN 4, a novel DWARF11 allele that affects brassinosteroid biosynthesis in rice. Sci Bull 60(10):905–915. https://doi.org/10.1007/s11434-015-0798-8
Sohrabi M, Rafii MY, Hanafi MM, Akmar ASN, Latif MA (2012) Genetic diversity of upland rice germplasm in Malaysia based on quantitative traits. Sci World J. https://doi.org/10.1100/2012/416291
Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, Segami S, Miura K, Ogawa D, Kamura T, Suzuki T, Higashiyama T, Yamasaki M, Mori H, Inukai Y, Wu J, Kitano H, Sakakibara H, Jacobsen SE, Ashikari M (2015) Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc Natl Acad Sci U S A 112(1):76–81. https://doi.org/10.1073/pnas.1421127112
Su S, Hong J, Chen X, Zhang C, Chen M, Luo Z, Chang S, Bai S, Liang W, Liu Q, Zhang D (2021) Gibberellins orchestrate panicle architecture mediated by DELLA-KNOX signalling in rice. Plant Biotechnol J 19(11):2304–2318. https://doi.org/10.1111/pbi.13661
Sun L, Li X, Fu Y, Zhu Z, Tan L, Liu F, Sun X, Sun X, Sun C (2013) GS6, a member of the GRAS gene family, negatively regulates grain size in rice. J Integr Plant Biol 55(10):938–949. https://doi.org/10.1111/jipb.12062
Sun S, Wang T, Wang L, Li X, Jia Y, Liu C, Huang X, Xie W, Wang X (2018) Natural selection of a GSK3 determines rice mesocotyl domestication by coordinating strigolactone and brassinosteroid signaling. Nat Commun 9(1):2523. https://doi.org/10.1038/s41467-018-04952-9
Sun K, Huang M, Zong W, Xiao D, Lei C, Luo Y, Song Y, Li S, Hao Y, Luo W, Xu B, Guo X, Wei G, Chen L, Liu YG, Guo J (2022) Hd1, Ghd7, and DTH8 synergistically determine the rice heading date and yield-related agronomic traits. J Genet Genomics 49(5):437–447. https://doi.org/10.1016/j.jgg.2022.02.018
Takano S, Matsuda S, Funabiki A, Furukawa J, Yamauchi T, Tokuji Y, Nakazono M, Shinohara Y, Takamure I, Kato K (2015) The rice RCN11 gene encodes beta1,2-xylosyltransferase and is required for plant responses to abiotic stresses and phytohormones. Plant Sci 236:75–88. https://doi.org/10.1016/j.plantsci.2015.03.022
Tanaka W, Ohmori Y, Ushijima T, Matsusaka H, Matsushita T, Kumamaru T, Kawano S, Hirano HY (2015) Axillary meristem formation in rice requires the WUSCHEL ortholog tillers absent1. Plant Cell 27(4):1173–1184. https://doi.org/10.1105/tpc.15.00074
Teoh CC, Zulkifli NA, Ong KK, Norliza AB, Abdul Rauf UF, Wan Yunus WMZ (2019) Influence of clinorotation on total grain yield per plant of MR 219 rice seed. Mater Today: Proc 19:1446–1450. https://doi.org/10.1016/j.matpr.2019.11.167
Tong X, Wang Y, Sun A, Bello BK, Ni S, Zhang J (2018) Notched belly grain 4, a novel allele of Dwarf 11, regulates grain shape and seed germination in rice (Oryza sativa L.). Int J Mol Sci. https://doi.org/10.3390/ijms19124069
Tu B, Tao Z, Wang S, Zhou L, Zheng L, Zhang C, Li X, Zhang X, Yin J, Zhu X, Yuan H, Li T, Chen W, Qin P, Ma B, Wang Y, Li S (2022) Loss of Gn1a/OsCKX2 confers heavy-panicle rice with excellent lodging resistance. J Integr Plant Biol 64(1):23–38. https://doi.org/10.1111/jipb.13185
Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38(16):e164. https://doi.org/10.1093/nar/gkq603
Wang H, Xu X, Vieira FG, Xiao Y, Li Z, Wang J, Nielsen R, Chu C (2016) The power of inbreeding: NGS-based GWAS of rice reveals convergent evolution during rice domestication. Mol Plant 9(7):975–985. https://doi.org/10.1016/j.molp.2016.04.018
Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153(4):1747–1758. https://doi.org/10.1104/pp.110.156943
Wu W, Zheng XM, Lu G, Zhong Z, Gao H, Chen L, Wu C, Wang HJ, Wang Q, Zhou K, Wang JL, Wu F, Zhang X, Guo X, Cheng Z, Lei C, Lin Q, Jiang L, Wang H, Ge S, Wan J (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(8):2775–2780. https://doi.org/10.1073/pnas.1213962110
Wu J, Feng F, Lian X, Teng X, Wei H, Yu H, Xie W, Yan M, Fan P, Li Y, Ma X, Liu H, Yu S, Wang G, Zhou F, Luo L, Mei H (2015) Genome-wide association study (GWAS) of mesocotyl elongation based on re-sequencing approach in rice. BMC Plant Biol 15:218. https://doi.org/10.1186/s12870-015-0608-0
Wu Y, Fu Y, Zhao S, Gu P, Zhu Z, Sun C, Tan L (2016) Clustered primary branch 1, a new allele of Dwarf11, controls panicle architecture and seed size in rice. Plant Biotechnol J 14(1):377–386. https://doi.org/10.1111/pbi.12391
Xia T, Chen H, Dong S, Ma Z, Ren H, Zhu X, Fang X, Chen F (2020) OsWUS promotes tiller bud growth by establishing weak apical dominance in rice. Plant J 104(6):1635–1647. https://doi.org/10.1111/tpj.15026
Xie X, Song MH, Jin F, Ahn SN, Suh JP, Hwang HG, McCouch SR (2006) Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon. Theor Appl Genet 113(5):885–894. https://doi.org/10.1007/s00122-006-0348-5
Xie X, Jin F, Song MH, Suh JP, Hwang HG, Kim YG, McCouch SR, Ahn SN (2008) Fine mapping of a yield-enhancing QTL cluster associated with transgressive variation in an Oryza sativa x O. rufipogon cross. Theor Appl Genet 116(5):613–622. https://doi.org/10.1007/s00122-007-0695-x
Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46(10):1674–1681. https://doi.org/10.1093/pcp/pci183
Xu C, Wang Y, Yu Y, Duan J, Liao Z, Xiong G, Meng X, Liu G, Qian Q, Li J (2012) Degradation of MONOCULM 1 by APC/C(TAD1) regulates rice tillering. Nat Commun 3:750. https://doi.org/10.1038/ncomms1743
Xu Y, Zong W, Hou X, Yao J, Liu H, Li X, Zhao Y, Xiong L (2015) OsARID3, an AT-rich Interaction Domain-containing protein, is required for shoot meristem development in rice. Plant J 83(5):806–817. https://doi.org/10.1111/tpj.12927
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(6):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(2):319–330. https://doi.org/10.1093/mp/ssq070
Yang GH, Xing YZ, Li SQ, Ding JZ, Yue B, Deng K, Li YS, Zhu YG (2006) Molecular dissection of developmental behavior of tiller number and plant height and their relationship in rice (Oryza sativa L.). Hereditas 143(1):236–245. https://doi.org/10.1111/j.2006.0018-0661.01959.x
Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88(1):76–82. https://doi.org/10.1016/j.ajhg.2010.11.011
Yang W, Guo Z, Huang C, Duan L, Chen G, Jiang N, Fang W, Feng H, Xie W, Lian X, Wang G, Luo Q, Zhang Q, Liu Q, Xiong L (2014) Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 5:5087. https://doi.org/10.1038/ncomms6087
Yang X, Zhao X, Dai Z, Ma F, Miao X, Shi Z (2021) OsmiR396/growth regulating factor modulate rice grain size through direct regulation of embryo-specific miR408. Plant Physiol 186(1):519–533. https://doi.org/10.1093/plphys/kiab084
Yang H, Yang Q, Kang Y, Zhang M, Zhan X, Cao L, Cheng S, Wu W, Zhang Y (2022) Finding stable QTL for plant height in super hybrid rice. Agriculture. https://doi.org/10.3390/agriculture12020165
Yu H, Murchie EH, Gonzalez-Carranza ZH, Pyke KA, Roberts JA (2015) Decreased photosynthesis in the erect panicle 3 (ep3) mutant of rice is associated with reduced stomatal conductance and attenuated guard cell development. J Exp Bot 66(5):1543–1552. https://doi.org/10.1093/jxb/eru525
Yu Y, Yu J, Wang Q, Wang J, Zhao G, Wu H, Zhu Y, Chu C, Fang J (2021) Overexpression of the rice ORANGE gene OsOR negatively regulates carotenoid accumulation, leads to higher tiller numbers and decreases stress tolerance in Nipponbare rice. Plant Sci 310:110962. https://doi.org/10.1016/j.plantsci.2021.110962
Zhang Y, Luo L, Xu C, Zhang Q, Xing Y (2006) Quantitative trait loci for panicle size, heading date and plant height co-segregating in trait-performance derived near-isogenic lines of rice (Oryza sativa). Theor Appl Genet 113(2):361–368. https://doi.org/10.1007/s00122-006-0305-3
Zhang L, Li Q, Dong H, He Q, Liang L, Tan C, Han Z, Yao W, Li G, Zhao H, Xie W, Xing Y (2015) Three CCT domain-containing genes were identified to regulate heading date by candidate gene-based association mapping and transformation in rice. Sci Rep 5:7663. https://doi.org/10.1038/srep07663
Zhang Z, Sun X, Ma X, Xu B, Zhao Y, Ma Z, Li G, Khan NU, Pan Y, Liang Y, Zhang H, Li J, Li Z (2021) GNP6, a novel allele of MOC1, regulates panicle and tiller development in rice. Crop J 9(1):57–67. https://doi.org/10.1016/j.cj.2020.04.011
Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) Elongated uppermost internode encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18(2):442–456. https://doi.org/10.1105/tpc.105.038455
Zhu X, Liang W, Cui X, Chen M, Yin C, Luo Z, Zhu J, Lucas WJ, Wang Z, Zhang D (2015) Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of carbon starved anther, a MYB domain protein. Plant J 82(4):570–581. https://doi.org/10.1111/tpj.12820
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 YG, Guo J (2021) Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading. New Phytol 229(3):1635–1649. https://doi.org/10.1111/nph.16946
Acknowledgements
The authors thank Delin Hong, State Key Laboratory of Crop Genetics and Germplasm Innovation, Nanjing Agricultural University, for providing the rice materials used in this study.
Funding
This research was funded by the Natural Science Foundation of Anhui Province, grant number 2108085MC97; National Natural Science Foundation of China, Grant Numbers 32101768 and U21A20214; Natural Science Foundation of Anhui Universities, Grant Number KJ2020A0118; Talent Project of Anhui Agricultural University, Grant Number rc312002; Natural Science Research Project of Colleges and Universities in Anhui Province, Grant Number YJS20210250; and Key Research and Development Program of Anhui Province, Grant Number 202004a06020024.
Author information
Authors and Affiliations
Contributions
XC, YC and EL designed the research, reviewed the writing and drafted the manuscript. YC, XC, JS, MZ, ZL, LL and HS participated in the experiments. MD and MX handled the germplasm. XC revised the manuscript. All the authors read the manuscript carefully and approved it.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest regarding the publication of this paper.
Human or animal rights
This study does not include human or animal subjects.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cheng, X., Chang, Y., Sun, J. et al. Identification of candidate genes and favourable haplotypes for yield traits in rice based on a genome-wide association study. Euphytica 219, 125 (2023). https://doi.org/10.1007/s10681-023-03253-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-023-03253-7