{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T23:54:46Z","timestamp":1789516486414,"version":"build-2803163510"},"reference-count":58,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,11,25]],"date-time":"2021-11-25T00:00:00Z","timestamp":1637798400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32060452"],"award-info":[{"award-number":["32060452"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32160447"],"award-info":[{"award-number":["32160447"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>Rice (<jats:italic>Oryza sativa<\/jats:italic> L.) is an important staple food crop for more than half of the world\u2019s population. Enhancing the grain quality and yield of rice to meet growing demand remains a major challenge. Here, we show that <jats:italic>OsMKK3<\/jats:italic> encode a MAP kinase kinase that controls grain size and chalkiness by affecting cell proliferation in spikelet hulls. We showed that <jats:italic>OsSPL16<\/jats:italic>, <jats:italic>GS5<\/jats:italic>, and <jats:italic>GIF1<\/jats:italic> have a substantial effect on the <jats:italic>OsMKK3<\/jats:italic>-regulated grain size pathway. <jats:italic>OsMKK3<\/jats:italic> has experienced strong directional selection in <jats:italic>indica<\/jats:italic> and <jats:italic>japonica<\/jats:italic>. Wild rice accessions contained four <jats:italic>OsMKK3<\/jats:italic> haplotypes, suggesting that the <jats:italic>OsMKK3<\/jats:italic> haplotypes present in cultivated rice likely originated from different wild rice accessions during rice domestication. <jats:italic>OsMKK3<\/jats:italic>-Hap1, <jats:italic>gs3<\/jats:italic>, and <jats:italic>gw8<\/jats:italic> were polymerized to enhance the grain length. Polymerization of beneficial alleles, such as <jats:italic>OsMKK3<\/jats:italic>-Hap1, <jats:italic>gs3<\/jats:italic>, <jats:italic>gw8<\/jats:italic>, <jats:italic>fgr<\/jats:italic>, <jats:italic>alk<\/jats:italic>, <jats:italic>chalk5<\/jats:italic>, and <jats:italic>wx<\/jats:italic>, also improved the quality of hybrid rice. Overall, the results indicated that beneficial <jats:italic>OsMKK3<\/jats:italic> alleles could be used for genomic-assisted breeding for rice cultivar improvement and be polymerized with other beneficial alleles.<\/jats:p>","DOI":"10.3389\/fpls.2021.784037","type":"journal-article","created":{"date-parts":[[2021,12,1]],"date-time":"2021-12-01T01:16:43Z","timestamp":1638321403000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":21,"title":["Natural Variation in OsMKK3 Contributes to Grain Size and Chalkiness in Rice"],"prefix":"10.3389","volume":"12","author":[{"given":"Yinghua","family":"Pan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haifeng","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingcheng","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muhammad Abdul Rehman","family":"Rashid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunju","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weiyong","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingka","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuntao","family":"Liang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hao","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongjing","family":"Qing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lijun","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gaoxing","family":"Dai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danting","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guofu","family":"Deng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,11,25]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"D1023","DOI":"10.1093\/nar\/gku1039","article-title":"SNP-Seek database of SNPs derived from 3000 rice genomes.","volume":"43","author":"Alexandrov","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"B2","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1126\/science.1113373","article-title":"Cytokinin oxidase regulates rice grain production.","volume":"309","author":"Ashikari","year":"2005","journal-title":"Science"},{"key":"B3","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/j.1467-7652.2005.00131.x","article-title":"The gene for fragrance in rice.","volume":"3","author":"Bradbury","year":"2005","journal-title":"Plant Biotechnol. J."},{"key":"B4","doi-asserted-by":"publisher","first-page":"621871","DOI":"10.3389\/fgene.2020.621871","article-title":"QTL mapping and identification of candidate genes for heat tolerance at the flowering stage in rice.","volume":"11","author":"Chen","year":"2021","journal-title":"Front. Genet."},{"key":"B5","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/j.tplants.2010.05.004","article-title":"Molecular basis of trait correlations.","volume":"15","author":"Chen","year":"2010","journal-title":"Trends Plant Sci."},{"key":"B6","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.rsci.2019.12.010","article-title":"Effects of GS3 and GL3.1 for grain size editing by CRISPR\/Cas9 in rice.","volume":"27","author":"Chen","year":"2020","journal-title":"Rice Sci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"2156","DOI":"10.1093\/bioinformatics\/btr330","article-title":"The variant call format and VCFtools.","volume":"27","author":"Danecek","year":"2011","journal-title":"Bioinform."},{"key":"B8","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1111\/tpj.12405","article-title":"SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice.","volume":"77","author":"Duan","year":"2014","journal-title":"Plant J."},{"key":"B9","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1016\/j.molp.2017.03.009","article-title":"Natural variation in the promoter of GSE5 contributes to grain size diversity in rice.","volume":"10","author":"Duan","year":"2017","journal-title":"Mol. Plant"},{"key":"B10","doi-asserted-by":"publisher","first-page":"1164","DOI":"10.1007\/s00122-006-0218-1","article-title":"GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein.","volume":"112","author":"Fan","year":"2006","journal-title":"Theor. Appl. Genet."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1353","DOI":"10.1016\/j.molp.2017.07.014","article-title":"Dissecting the genetic basis of grain shape and chalkiness traits in hybrid rice using multiple collaborative populations.","volume":"10","author":"Gong","year":"2017","journal-title":"Mol. Plant"},{"key":"B12","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1016\/0140-6736(90)92086-w","article-title":"Genotyping of poor metabolisers of debrisoquine by allele-specific PCR amplification.","volume":"336","author":"Heim","year":"1990","journal-title":"Lancet"},{"key":"B13","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1038\/nature11532","article-title":"A map of rice genome variation reveals the origin of cultivated rice.","volume":"490","author":"Huang","year":"2012","journal-title":"Nature"},{"key":"B14","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1038\/ng.2612","article-title":"Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield.","volume":"45","author":"Ishimaru","year":"2013","journal-title":"Nat. Genet."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: molecular evolutionary genetics analysis Version 7.0 for bigger datasets.","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1111\/pbi.13177","article-title":"Using Heading date 1 preponderant alleles from indica cultivars to breed high-yield, high-quality japonica rice varieties for cultivation in south China.","volume":"18","author":"Leng","year":"2020","journal-title":"Plant Biotechnol. J."},{"key":"B17","doi-asserted-by":"publisher","first-page":"W256","DOI":"10.1093\/nar\/gkz239","article-title":"Interactive Tree Of Life (iTOL) v4: recent updates and new developments.","volume":"47","author":"Letunic","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"B18","doi-asserted-by":"publisher","first-page":"650","DOI":"10.3389\/fpls.2018.00650","article-title":"Genetic basis underlying correlations among growth duration and yield traits revealed by GWAS in rice (Oryza sativa L.).","volume":"9","author":"Li","year":"2018","journal-title":"Front. Plant Sci."},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1101\/2020.06.04.134023","article-title":"Combination of favorable gene haplotypes plays an important role in rice hybrid grain quality traits based on genome-wide association analysis.","author":"Li","year":"2020","journal-title":"bioRxiv"},{"key":"B20","doi-asserted-by":"publisher","first-page":"1266","DOI":"10.1038\/ng.977","article-title":"Natural variation in GS5 plays an important role in regulating grain size and yield in rice.","volume":"43","author":"Li","year":"2011","journal-title":"Nat. Genet."},{"key":"B21","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1038\/ng.2923","article-title":"Chalk5 encodes a vacuolar H(+)\u2013translocating pyrophosphatase influencing grain chalkiness in rice.","volume":"46","author":"Li","year":"2014","journal-title":"Nat. Genet."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1451","DOI":"10.1093\/bioinformatics\/btp187","article-title":"DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.","volume":"25","author":"Librado","year":"2009","journal-title":"Bioinform."},{"key":"B23","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1038\/s41467-018-03047-9","article-title":"G-protein \u03b2\u03b3 subunits determine grain size through interaction with MADS-domain transcription factors in rice.","volume":"9","author":"Liu","year":"2018","journal-title":"Nat. Commun."},{"key":"B24","doi-asserted-by":"publisher","first-page":"19579","DOI":"10.1073\/pnas.1014419107","article-title":"Linking differential domain functions of the GS3 protein to natural variation of grain size in rice.","volume":"107","author":"Mao","year":"2010","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B25","doi-asserted-by":"publisher","first-page":"2008","DOI":"10.1093\/mp\/sst121","article-title":"Application of the CRISPR-Cas system for efficient genome engineering in plants.","volume":"6","author":"Mao","year":"2013","journal-title":"Mol. Plant"},{"key":"B26","doi-asserted-by":"crossref","first-page":"2503","DOI":"10.1093\/nar\/17.7.2503","article-title":"Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS).","volume":"17","author":"Newton","year":"1989","journal-title":"Nucleic Acids Res."},{"key":"B27","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1038\/ncomms1132","article-title":"New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield.","volume":"1","author":"Ookawa","year":"2010","journal-title":"Nat. Commun."},{"key":"B28","first-page":"498","article-title":"Genetic structure and core collection of common wild rice (Oryza rufipogon Griff.) in Guangxi.","volume":"19","author":"Pan","year":"2018","journal-title":"J. Plant Genet."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s12374-020-09290-2","article-title":"OrMKK3 influences morphology and grain size in rice.","volume":"4","author":"Pan","year":"2021","journal-title":"J. Plant Biol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1666","DOI":"10.1038\/cr.2012.151","article-title":"The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3.","volume":"22","author":"Qi","year":"2012","journal-title":"Cell Res."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1038\/ng.169","article-title":"Deletion in a gene associated with grain size increased yields during rice domestication.","volume":"40","author":"Shomura","year":"2008","journal-title":"Nat. Genet."},{"key":"B32","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1038\/ng.3518","article-title":"OsSPL13 controls grain size in cultivated rice.","volume":"48","author":"Si","year":"2016","journal-title":"Nat. Genet."},{"key":"B33","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1073\/pnas.1421127112","article-title":"Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice.","volume":"112","author":"Song","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1745-459x.2007.00129.x","article-title":"Rice-eating quality among consumers in different rice grain preference countries.","volume":"23","author":"Suwannaporn","year":"2008","journal-title":"J. Sens. Stud."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1534\/genetics.109.103002","article-title":"Evolutionary history of GS3, a gene conferring grain length in rice.","volume":"182","author":"Takano-Kai","year":"2009","journal-title":"Genet."},{"key":"B36","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1111\/jipb.12745","article-title":"GW5-Like, a homolog of GW5, negatively regulates grain width, weight and salt resistance in rice.","volume":"61","author":"Tian","year":"2019","journal-title":"J. Integr. Plant Biol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"21760","DOI":"10.1073\/pnas.0912396106","article-title":"Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities.","volume":"106","author":"Tian","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B38","doi-asserted-by":"publisher","first-page":"949","DOI":"10.1038\/ng.3352","article-title":"The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality.","volume":"47","author":"Wang","year":"2015","journal-title":"Nat. Genet."},{"key":"B39","doi-asserted-by":"publisher","first-page":"950","DOI":"10.1038\/ng.2327","article-title":"Control of grain size, shape and quality by OsSPL16 in rice.","volume":"44","author":"Wang","year":"2012","journal-title":"Nat. Genet."},{"key":"B40","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1038\/s41586-018-0063-9","article-title":"Genomic variation in 3,010 diverse accessions of Asian cultivated rice.","volume":"557","author":"Wang","year":"2018","journal-title":"Nature"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1747","DOI":"10.1104\/pp.110.156943","article-title":"DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously.","volume":"153","author":"Wei","year":"2010","journal-title":"Plant Physiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/j.jgg.2018.03.007","article-title":"The rational design of multiple molecular module-based assemblies for simultaneously improving rice yield and grain quality.","volume":"45","author":"Wu","year":"2018","journal-title":"J.Genet. Genomics"},{"key":"B43","doi-asserted-by":"publisher","first-page":"754","DOI":"10.1016\/j.molp.2018.03.006","article-title":"GL3.3, a novel QTL encoding a GSK3\/SHAGGY-like Kinase, epistatically interacts with GS3 to produce extra-long grains in rice.","volume":"11","author":"Xia","year":"2018","journal-title":"Mol. Plant"},{"key":"B44","doi-asserted-by":"publisher","first-page":"761","DOI":"10.1038\/ng.143","article-title":"Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice.","volume":"40","author":"Xue","year":"2008","journal-title":"Nat. Genet."},{"key":"B45","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1093\/mp\/ssq070","article-title":"A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice.","volume":"4","author":"Yan","year":"2011","journal-title":"Mol. Plant"},{"key":"B46","doi-asserted-by":"publisher","first-page":"e0196690","DOI":"10.1371\/journal.pone.0196690","article-title":"Identification of candidate genes for gelatinization temperature, gel consistency and pericarp color by GWAS in rice based on SLAF-sequencing.","volume":"13","author":"Yang","year":"2018","journal-title":"PLoOne"},{"key":"B47","doi-asserted-by":"publisher","first-page":"2473","DOI":"10.1105\/tpc.12.12.2473","article-title":"Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS.","volume":"12","author":"Yano","year":"2000","journal-title":"Plant Cell"},{"key":"B48","doi-asserted-by":"publisher","first-page":"891","DOI":"10.1111\/j.1365-313X.2007.03284.x","article-title":"TAC1, a major quantitative trait locus controlling tiller angle in rice.","volume":"52","author":"Yu","year":"2007","journal-title":"Plant J."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1667","DOI":"10.1111\/pbi.12903","article-title":"Alternative splicing of OsLG3b controls grain length and yield in japonica rice.","volume":"16","author":"Yu","year":"2018","journal-title":"Plant Biotechnol. J."},{"key":"B50","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1186\/s12915-017-0365-7","article-title":"OsLG3 contributing to rice grain length and yield was mined by Ho-LAMap.","volume":"15","author":"Yu","year":"2017","journal-title":"BMC Biol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"17031","DOI":"10.1038\/nplants.2017.31","article-title":"Rational design of high-yield and superior-quality rice.","volume":"3","author":"Zeng","year":"2017","journal-title":"Nat. Plants"},{"key":"B52","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.molp.2021.02.003","article-title":"The landscape of gene\u2013CDS\u2013haplotype diversity in rice: properties, population organization, footprints of domestication and breeding, and implications for genetic improvement.","volume":"14","author":"Zhang","year":"2021","journal-title":"Mol. Plant"},{"key":"B53","doi-asserted-by":"publisher","first-page":"110208","DOI":"10.1016\/j.plantsci.2019.110208","article-title":"Small Grain and Dwarf 2, encoding an HD-Zip II family transcription factor, regulates plant development by modulating gibberellin biosynthesis in rice.","volume":"288","author":"Zhang","year":"2019","journal-title":"Plant Sci."},{"key":"B54","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1007\/s11032-020-01161-5","article-title":"Exploration and selection of elite Sd1 alleles for rice design breeding.","volume":"40","author":"Zhang","year":"2020","journal-title":"Mol. Breed."},{"key":"B55","doi-asserted-by":"publisher","first-page":"16402","DOI":"10.1073\/pnas.0708013104","article-title":"Strategies for developing Green super rice.","volume":"104","author":"Zhang","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B56","doi-asserted-by":"publisher","first-page":"21534","DOI":"10.1073\/pnas.1219776110","article-title":"Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice.","volume":"109","author":"Zhang","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B57","doi-asserted-by":"publisher","first-page":"12844","DOI":"10.1073\/pnas.1615104113","article-title":"Critical roles of soluble starch synthase SSIIIa and granule-bound starch synthase Waxy in synthesizing resistant starch in rice.","volume":"113","author":"Zhou","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B58","doi-asserted-by":"publisher","first-page":"80","DOI":"10.16267\/j.cnki.1005-3956.20190226.049","article-title":"Wantaiyou 3158, a new super hybrid rice combination for both early and late season.","volume":"34","author":"Zhou","year":"2019","journal-title":"Hybrid Rice"}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2021.784037\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,1]],"date-time":"2021-12-01T01:16:51Z","timestamp":1638321411000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2021.784037\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,25]]},"references-count":58,"alternative-id":["10.3389\/fpls.2021.784037"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2021.784037","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,25]]},"article-number":"784037"}}