玉米花期根系结构的表型变异与全基因组关联分析
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摘要
【目的】根系作为植株吸收水分和养分的重要器官,对玉米生长及产量的形成至关重要。研究玉米根系结构的遗传机制指导玉米高产育种实践。【方法】以111份玉米优异自交系为材料,于2017年在北京、陕西永寿、山西定襄和河南原阳4个环境下对玉米地下节根层数(RLN)、地下节根总条数(TRN)、地下节根角度(RA)、地下节根面积(RS)、地下节根体积(RV)和地下节根干重(RDW)等6个玉米根系相关性状进行调查。取4个环境的平均值作为6个根系相关性状的表型数据,对6个相关性状进行统计分析和相关性分析,对不同年代、不同类群自交系的地下节根相关性状进行差异分析。基于该群体全基因组152 352个高质量SNP标记,利用FarmCPU模型进行全基因组关联分析获得显著关联SNP位点,并在LD衰减距离范围内查找候选基因,对候选基因的功能进行富集分析。【结果】表型分析表明,6个地下节根性状均呈现正态分布,且均显示出较高的遗传力;相关性分析结果表明,地下节根层数和总条数均与地下节根角度和面积呈负相关,地下节根的角度、面积、体积和干重等4个性状之间相互呈现显著正相关关系;不同年代的玉米地下根系结构存在差异,地下节根层数和总条数在年代的更替间表现出下降的趋势,地下节根角度和面积在年代更替间表现出上升的趋势,根干重和根体积在各年代间无显著差异;玉米地下根系结构在类群间也存在差异,旅大红骨类群的6个地下节根性状值均高于其余类群。全基因组关联分析共检测到26个SNP位点与地下节根层数、总条数、体积和干重性状显著关联(P<0.00001),其中11个显著关联位点定位于前人报道的根系QTL区间内,2个显著关联SNP在地下节根层数和总条数中均被检测到。基于显著关联SNP位点共挖掘到177个候选基因,其中135个具有功能注释,Zm00001d037368可能为控制地下节根层数和总条数的一因多效候选基因。候选基因功能的富集分析结果显示,候选基因的功能主要涉及植物体内的代谢调节、应激反应、运输活性、催化活性、结合蛋白及细胞成分等。【结论】玉米自交系的根系结构在不同年代间和不同类群间存在不同程度的差异,采用全基因组关联分析策略挖掘控制玉米根系结构的相关遗传位点及候选基因,共检测到26个显著关联的SNP位点。
【Objective】The root system as an important organ absorbing water and nutrients for plants, is essential for growth and grain yield of maize. More understanding of the genetic mechanism of the root architecture of maize is of great significance for the practice of high-yield breeding of maize.【Method】In this study, 111 maize elite inbred lines were used as an association population. In 2017, six belowground nodal root-related traits, i.e. nodal root layer number(RLN), total nodal root number(TRN),nodal root angle(RA), nodal root area(RS), nodal root volume(RV) and nodal root dry weight(RDW), were measured under four environments including Beijing, Yongshou of Shanxi province, Dingxiang of Shanxi province and Yuanyang of Henan province. The average of the four environments were used as the phenotypic data of the six root-related traits. The statistical analysis and correlation analysis were carried out on six traits, and the differences of six root-related traits for inbred lines developed in different eras and for inbred lines in different heterotic groups were also analyzed. Based on 152352 high-quality SNP markers obtained in this population, the Farm CPU model was used for genome-wide association analysis to obtain significantly associated SNP loci, and candidate genes were predicted based on the LD interval sequence of these significant associated SNPs, and a functional enrichment analysis of candidate genes was carried out.【Result】The phenotypic analysis showed that the six belowground nodal root traits exhibited a normal distribution and high level of heritability. The correlation analysis showed that RLN and TRN are negatively correlated with RA and RS; RA, RS, RV and RDW are significantly positively correlated with each other. With the advance of maize breeding era, RLN and TRN had a decreasing trend, and RA and RS had an increasing trend. There were no significant differences for RDW and RV among inbred lines of different eras. The belowground root structure of those inbred lines from different maize heterotic groups also showed differences, and the six traits of the Lüda Red Cob group were all higher than those of other groups.Genome-wide association study(GWAS) yielded 26 significantly associated SNPs(P<0.00001) referring to RLN, TRN, RV and RDW, of which 11 SNPs located in root-related QTLs previously reported, and 2 SNPs were detected to be significant correlation with RLN and TRN. A total of 177 candidate genes were found based on those significantly associated SNPs, of which 135 genes have functional annotation, the gene Zm00001 d037368 was one pleiotropic gene influencing RLN and TRN. The results of enrichment analysis of candidate genes mainly involved in metabolic regulation, the response to stress, transporter activity, catalytic activity, binding protein and cellular components in plants.【Conclusion】The root architecture of maize inbred lines from different eras and different heterotic groups had differences with various degree. Root-related genetic loci and candidate genes identified by the genome-wide association analysis, a total of 26 loci associated with root-related traits were identified.
【Objective】The root system as an important organ absorbing water and nutrients for plants, is essential for growth and grain yield of maize. More understanding of the genetic mechanism of the root architecture of maize is of great significance for the practice of high-yield breeding of maize.【Method】In this study, 111 maize elite inbred lines were used as an association population. In 2017, six belowground nodal root-related traits, i.e. nodal root layer number(RLN), total nodal root number(TRN),nodal root angle(RA), nodal root area(RS), nodal root volume(RV) and nodal root dry weight(RDW), were measured under four environments including Beijing, Yongshou of Shanxi province, Dingxiang of Shanxi province and Yuanyang of Henan province. The average of the four environments were used as the phenotypic data of the six root-related traits. The statistical analysis and correlation analysis were carried out on six traits, and the differences of six root-related traits for inbred lines developed in different eras and for inbred lines in different heterotic groups were also analyzed. Based on 152352 high-quality SNP markers obtained in this population, the Farm CPU model was used for genome-wide association analysis to obtain significantly associated SNP loci, and candidate genes were predicted based on the LD interval sequence of these significant associated SNPs, and a functional enrichment analysis of candidate genes was carried out.【Result】The phenotypic analysis showed that the six belowground nodal root traits exhibited a normal distribution and high level of heritability. The correlation analysis showed that RLN and TRN are negatively correlated with RA and RS; RA, RS, RV and RDW are significantly positively correlated with each other. With the advance of maize breeding era, RLN and TRN had a decreasing trend, and RA and RS had an increasing trend. There were no significant differences for RDW and RV among inbred lines of different eras. The belowground root structure of those inbred lines from different maize heterotic groups also showed differences, and the six traits of the Lüda Red Cob group were all higher than those of other groups.Genome-wide association study(GWAS) yielded 26 significantly associated SNPs(P<0.00001) referring to RLN, TRN, RV and RDW, of which 11 SNPs located in root-related QTLs previously reported, and 2 SNPs were detected to be significant correlation with RLN and TRN. A total of 177 candidate genes were found based on those significantly associated SNPs, of which 135 genes have functional annotation, the gene Zm00001 d037368 was one pleiotropic gene influencing RLN and TRN. The results of enrichment analysis of candidate genes mainly involved in metabolic regulation, the response to stress, transporter activity, catalytic activity, binding protein and cellular components in plants.【Conclusion】The root architecture of maize inbred lines from different eras and different heterotic groups had differences with various degree. Root-related genetic loci and candidate genes identified by the genome-wide association analysis, a total of 26 loci associated with root-related traits were identified.
引文
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[2]VILLORDON A Q,GINZBERG I,FIRON N.Root architecture and root and tuber crop productivity.Trends in Plant Science,2014,19(7):419-425.
[3]NING P,Li S,WHITE P J,LI C J.Maize varieties released in different eras have similar root length density distributions in the soil,which are negatively correlated with local concentrations of soil mineral nitrogen.PLoS ONE,2014,10(3):e0121892.
[4]HAMMER G L,DONG Z S,MCLEAN G,DOHERTY A,MESSINAC,SCHUSSLER J,ZINSELMEIER C,PASZKIEWICZ S,COOPERM.Can changes in canopy and/or root system architecture explain historical maize yield trends in the U.S.Corn belt?Crop Science,2009,49(1):299-312.
[5]CAI H G,CHEN F J,MI G H,ZHANG F S,MAURER H P,LIU WX,REIF J C,YUAN L X.Mapping QTLs for root system architecture of maize(Zea mays L.)in the field at different developmental stages.Theoretical and Applied Genetics,2012,125(6):1313-1324.
[6]程帅,李鹏程,刘志刚,赵龙飞,米国华.密度、氮肥对玉米杂交种节根数量的影响.植物营养与肥料学报,2016,22(4):1118-1125.CHENG S,LI P C,LIU Z G,ZHAO L F,MI G H.Effect of plant density and nitrogen supply on nodal root number of maize of different varieties.Journal of Plant Nutrition and Fertilizer,2016,22(4):1118-1125.(in Chinese)
[7]ALI M L,LUETCHENS J,NASCIMENTO J,SHAVER T M,KRUGER G R,LORENZ A J.Genetic variation in seminal and nodal root angle and their association with grain yield of maize under water-stressed field conditions.Plant Soil,2015,397(1/2):213-225.
[8]UGA Y,SUGIMOTO K,OGAWA S,RANE J,ISHITANI M,HARAN,KITOMI Y,INUKAI Y,ONO K,KANNO N,INOUE H,TAKEHISA H,MOTOYAMA R,NAGAMURA Y,WU J Z,MATSUMOTO T,TAKAI T,OKUNO K,YANO M.Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.Nature Genetics,2013,45(9):1097-1102.
[9]COMAS L H,BECKER S R,CRUZ V M V,BYRNE P F,DIERIG DA.Root traits contributing to plant productivity under drought.Frontiers in Plant Science,2013,4(2):442.
[10]GAO Y Z,LYNCH J P.Reduced crown root number improves water acquisition under water deficit stress in maize(Zea mays L.).Journal of Experimental Botany,2016,67(15):4545-4557.
[11]BURTON A L,JOHNSON J M,FOERSTER J M,HIRSCH C N,BUELL C R,HANLON M T,KAEPPLER S M,BROWN K M,LYNCH J P.QTL mapping and phenotypic variation for root architectural traits in maize(Zea mays L.).Theoretical and Applied Genetics,2014,127(11):2293-2311.
[12]KUMAR B,ABDEL-GHANI A H,PACE J,REYES-MATAMOROSJ,HOCHHOLDINGER F,LüBBERSTEDT T.Association analysis of single nucleotide polymorphisms in candidate genes with root traits in maize(Zea mays L.)seedlings.Plant Science,2014,224(13):9-19.
[13]PACE J,GARDNER C,ROMAY C,GANAPATHYSUBRAMANIAN B,LüBBERSTEDT T.Genome-wide association analysis of seedling root development in maize(Zea mays L.).BMC Genomics,2015,16(1):47.
[14]HOCHHOLDINGER F.The maize root system:Morphology,anatomy,and genetics//Handbook of Maize:Its Biology.New York:Springer,2009:145-160.
[15]ZHANG F L,NIU X K,ZHANG Y M,XIE R Z,LIU X,LI S K,GAO S J.Studies on the root characteristics of maize varieties of different eras.Journal of Integrative Agriculture,2013,12(3):426-435.
[16]ZAIDI P H,SEETHARAM K,KRISHNA G,KRISHNAMURTHY L,GAJANAN S,BABU R,ZERKA M,VINAYAN M T,VIVEK B S.Genomic regions associated with root traits under drought stress in tropical maize(Zea mays L.).PLoS ONE,2016,11(10):e0164340.
[17]ZHANG Z H,ZHANG X,LIN Z L,WANG J,XU M L,LAI J S,YUJ M,LIN Z W.The genetic architecture of nodal root number in maize.The Plant Journal,2018,93(6):1032-1044.
[18]ALI M L,LUETCHENS J,SINGH A,SHAVER T M,KRUGER G R,LORENZ A J.Greenhouse screening of maize genotypes for deep root mass and related root traits and their association with grain yield under water-deficit conditions in the field.Euphytica,2016,207(1):79-94.
[19]LANDI P,GIULIANI S,SALVI S,FERRI M,TUBEROSA R,SANGUINETI M C.Characterization of root-yield-1.06,a major constitutive QTL for root and agronomic traits in maize across water regimes.Journal of Experimental Botany,2010,61(13):3553-3562.
[20]蔡红光,刘建超,米国华,袁力行,陈晓辉,陈范骏,张福锁.田间条件下控制玉米开花前后根系性状的QTL定位.植物营养与肥料学报,2011,17(2):317-324.CAI H G,LIU J C,MI G H,YUAN L X,CHEN X H,CHEN F J,ZHANG F S.QTL mapping for root traits around flowering stage of maize under field condition.Journal of Plant Nutrition and Fertilizer,2011,17(2):317-324.(in Chinese)
[21]KU L X,SUN Z H,WANG C L,ZHANG J,ZHAO R F,LIU H Y,TAI G Q,CHEN Y H.QTL mapping and epistasis analysis of brace root traits in maize.Molecular Breeding,2012,30(2):697-708.
[22]GU D D,MEI X P,YU T T,SUN N N,XU D,LIU C X,CAI Y L.QTL identification for brace-root traits of maize in different generations and environments.Crop Science,2017,57:13-21.
[23]GUO J,CHEN L,LI Y X,SHI Y S,SONG Y C,ZHANG D F,LI Y,WANG T Y,YANG D G,LI C H.Meta-QTL analysis and identification of candidate genes related to root traits in maize.Euphytica,2018,214(12):223.
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