Genetic structure, gene flow pattern, and association analysis of superior germplasm resources in domesticated upland cotton (Gossypium hirsutum L.)

doi:10.1016/j.pld.2020.03.001

Abstract

Abstract: Gene flow patterns and the genetic structure of domesticated crops like cotton are not well understood. Furthermore, marker-assisted breeding of cotton has lagged far behind that of other major crops because the loci associated with cotton traits such as fiber yield and quality have scarcely been identified. In this study, we used 19 microsatellites to first determine the population genetic structure and patterns of gene flow of superior germplasm resources in upland cotton. We then used association analysis to identify which markers were associated with 15 agronomic traits (including ten yield and five fiber quality traits). The results showed that the upland cotton accessions have low levels of genetic diversity (polymorphism information content =0.427), although extensive gene flow occurred among different ecological and geographic regions. Bayesian clustering analysis indicated that the cotton resources used in this study did not belong to obvious geographic populations, which may be the consequence of a single source of domestication followed by frequent genetic introgression mediated by human transference. A total of 82 makeretrait associations were examined in association analysis and the related ratios for phenotypic variations ranged from 3.04% to 47.14%. Interestingly, nine SSR markers were detected in more than one environmental condition. In addition, 14 SSR markers were co-associated with two or more different traits. It was noteworthy that NAU4860 and NAU5077 markers detected at least in two environments were simultaneously associated with three fiber quality traits (uniformity index, specific breaking strength and micronaire value). In conclusion, these findings provide new insights into the population structure and genetic exchange pattern of cultivated cotton accessions. The quantitative trait loci of domesticated cotton identified will also be very useful for improvement of yield and fiber quality of cotton in molecular breeding programs.

Key words: Domestication cotton, Fiber quality traits, Genetic exchange, Microsatellite markers, Yield

Ting-Ting Zhang, Na-Yao Zhang, Wei Li, Xiao-Jian Zhou, Xiao-Yu Pei, Yan-Gai Liu, Zhong-Ying Ren, Kun-Lun He, Wen-Sheng Zhang, Ke-Hai Zhou, Fei Zhang, Xiong-Feng Ma, Dai-Gang Yang, Zhong-Hu Li. Genetic structure, gene flow pattern, and association analysis of superior germplasm resources in domesticated upland cotton (Gossypium hirsutum L.)[J]. Plant Diversity, 2020, 42(03): 189-197.

References

Abdalla, A.M., Reddy, O.U.K., Ei-Zik, K.M., Pepper, A.E., 2001. Genetic diversity and relationships of diploid and tetraploid cottons revealed using AFLP. Theor. Appl. Genet. 102, 222-229.
Abdurakhmonov, I.Y., Saha, S., Jenkins, J.N., Buriev, Z.T., Shermatov, S.E., Scheffler, B.E., Pepper, A.E., Yu, J.Z., Russell, J.K., Abdukarimov, A., 2009.
A Linkage disequilibrium based association mapping of fiber quality traits in G. hirsutum L. variety germplasm. Genetica 136, 401-417.
Ademe, M.S., He, S., Pan, Z., Sun, J.L., Wang, Q.L., Qin, H.D., Liu, J.H., Liu, H., Yang, J., Xu, D.Y., Yang, J.L., Ma, Z.Y., Zhang, J.B., Li, Z.K., Cai, Z.M., Zhang, X.L., Zhang, X., Huang, A.F., Yi, X.D., Zhou, G.Y., Li, L., Zhu, H.Y., Pang, B.Y., Wang, L.R., Jia, Y.H., Du, X.M., 2017. Association mapping analysis of fiber yield and quality traits in upland cotton (Gossypium hirsutum L.). Mol. Gen. Genet. 292, 1267-1280.
Adhikari, J., Das, S., Wang, Z.N., Khanal, S., Chandnani, R., Patel, J.D., Goff, V.H., Auckland, S., Rainville, L.K., Jones, D., Paterson, A.H., 2017. Targeted identification of association between cotton fiber quality traits and microsatellite markers. Euphytica 213, 65.
Beerli, P., Felsenstein, J., 1999. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152, 763-773.
Bradbury, P.J., Zhang, Z.W., 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.
Brown, W.L., 1983. Genetic diversity and genetic vulnerability-an appraisal. Econ. Bot. 37, 4-12.
Brubaker, C.L., Wendel, J.F., 1994. Re-evaluating the origin of domesticated cotton(Gossypium hirsutum; Malvaceae) using nuclear restriction fragment length polymorphism (RFLP). Am. J. Bot. 81, 1309-1326.
Cai, C.P., Ye, W.X., Zhang, T.Z., Guo, W.Z., 2014. Association analysis of fiber quality traits and exploration of elite alleles in Upland cotton cultivars/accessions(Gossypium hirsutum L.). J. Integr. Plant Biol. 56, 51-62.
Campbell, B.T., Saha, S., Percy, R., Frelichowski, J., Jenkins, J.N., Park, W., Mayee, C.D., Gotmare, V., Dessauw, D., Giband, M., Jia, X.D.Y., Constable, G., Dillon, S., Abdurakhmonov, I.Y., Abdukarimov, A., Rizaeva, S.M., Abdullaev, A., Barroso, P.A.V., Pádua, J.G., Hoffmann, L.V., Podolnaya, L., 2010. Status of the global cotton germplasm resources. Crop Sci. 50, 1161-1179.
Cao, K., Zheng, Z.J., Wang, L.R., Liu, X., Zhu, G.G., Fang, W.C., Cheng, S.F., Zeng, P., Chen, C.W., Wang, X.W., Xie, M., Zhong, X., Wang, X.L., Zhao, P., Bian, C., Zhu, Y.L., Zhang, J.H., Ma, G.S., Chen, C.X., Li, Y.J., Hao, F.G., Li, Y., Huang, G.D., Li, Y.X., Li, H.Y., Guo, J., Xu, X., Wang, J., 2014. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 15, 415.
Cardon, L.R., Palmer, L.J., 2003. Population stratification and spurious allelic association. Lancet 361, 598-604.
Chen, G., Du, X.M., 2006. Genetic diversity of source germplasm of upland cotton in China as determined by SSR marker analysis. Acta Genetica Sin. 33, 733-745.
Coppens d'Eeckenbrugge, G., Lacape, J.M., 2014. Distribution and differentiation of wild, feral, and cultivated populations of perennial upland cotton (Gossypium hirsutum L.) in Mesoamerica and the Caribbean. PloS One 9, e107458.
Dong, C.G., Wang, J., Chen, Q.J., Yu, Y., Li, B.C., 2018a. Detection of favorable alleles for yield and yield components by association mapping in upland cotton. Genes Genome 40, 725-734.
Dong, C.G., Wang, J., Yu, Y., Li, B.C., 2018b. Association mapping and favorable QTL alleles for fiber quality traits in upland cotton (Gossypium hirsutum L.). J. Genet. 97, 1-12.
Dong, N., Li, C.Q., Wang, Q.L., Ai, N.J., Hu, G.H., Zhang, J.B., 2010. Mixed inheritance of earliness and its related traits of short-season cotton under different ecological enviroments. Acta Gossypii Sinica 22, 304-311.
Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
Earl, D.A., Vonholdt, B.M., 2012. Structure HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359-361.
Esbroeck, G.A.V., Bowman, D.T., May, O.L., Calhoun, D.S., 1999. Genetic similarity indices for ancestral cotton cultivars and their impact on genetic diversity estimates of modern cultivars. Crop Sci. 39, 323-328.
Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611-2620.
Excoffier, L., Lischer, H.E.L., 2010. Arlequin suite v. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564-567.
Fang, D.D., Hinze, L.L., Percy, R.G., Li, P., Deng, D., Thyssen, G., 2013. A microsatellitebased genome-wide analysis of genetic diversity and linkage disequilibrium in Upland cotton (Gossypium hirsutum L.) cultivars from major cotton-growing countries. Euphytica 191, 391-401.
Fang, L., Guan, X.Y., Zhang, T.Z., 2017. Asymmetric evolution and domestication in allotetraploid cotton (Gossypium hirsutum L.). Crop J 5, 159-165.
Flint-Garcia, S.A., Thuillet, A.C., Yu, J.M., Pressoir, G., Romero, S.M., Mitchell, S.E., Doebley, J., Kresovich, S., Goodman, M.M., Buckler, E.S., 2005. Maize association population: a higher solution platform for quantitative trait locus dissection. Plant J. 44, 1054-1064.
Guo, W.Z., Zhang, T.Z., Pan, J.J., Wang, X.Y., 1997. A preliminary study on genetic diversity of Upland cotton cultivars in China. Acta Gossypii Sinica 9, 19-24.
Gutiérrez, O.A., Basu, S., Saha, S., Jenkins, J.N., Shoemaker, D.B., Cheatham, C.L., McCarty, J.C., 2002. Genetic distance among selected cotton genotypes and its relationship with F2 performance. Crop Sci. 42, 1841-1847.
Handi, S.S., Katageri, I.S., Adiger, S., Jadhav, M.P., Lekkala, S.P., Lachagari, V.B.R., 2017. Association mapping for seed cotton yield, yield components and fibre quality traits in upland cotton (Gossypium hirsutumL.) genotypes. Plant Breed. 136, 958-968.
Holland, M.M., Parson, W., 2011. GeneMarker? HID: a reliable software tool for the analysis of forensic STR data. J. Forensic Sci. 56, 29-35.
Huang, C., Shen, C., Wen, T.W., Gao, B., Zhu, D., Li, X.F., Ahmed, M.M., Li, D.G., Lin, Z.X., 2018. SSR-based association mapping of fiber quality in upland cotton using an eight-way MAGIC population. Mol. Gen. Genet. 293, 793-805.
Iqbal, M.J., Reddy, O.U.K., El-Zik, K.M., Pepper, A.E., 2001. A geneticbottleneck in the ‘evolution under domestication’ of UplandcottonGossypium hirsutum L. examined using DNA fingerprinting. Theor. Appl. Genet. 103, 547-554.
Iqbal, M.J., Aziz, N., Saeed, N.A., Zafar, Y., Malik, K.A., 1997. Genetic diversity evaluation of some elite cotton varieties by RAPD analysis. Theor. Appl. Genet. 94, 139-144.
Islam, M.S., Thyssen, G.N., Jenkins, J.N., Zeng, L., Delhom, C.D., McCarty, J.C., Deng, D.D., Hinchliffe, D.J., Jones, D.C., Fang, D.D., 2016. A MAGIC populationbased genome-wideassociation study reveals functionalassociation of GhRBB1_A07 gene with superior fiber quality in cotton. BMC Genom. 17, 903.
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.
Kalinowski, S.T., Taper, M.L., Marshall, T.C., 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099-1106.
Keerio, A.A., Shen, C., Nie, Y.C., Ahmed, M.M., Zhang, X.L., Lin, Z.X., 2018. QTL mapping for fiber quality and yield traits based on introgression lines derived from Gossypium hirsutum×G. tomentosum. Int. J. Mol. Sci. 19, 243.
Lacape, J.M., Dessauw, D., Rajab, M., Noye, J.L., Hau, B., 2007. Microsatellite diversity in tetraploid Gossypium germplasm: assembling a highly informative genotyping set of cotton SSRs. Mol. Breed. 19, 45-58.
Lehner, B., 2011. Molecular mechanisms of epistasis within and between genes. Trends Genet. 27, 323-331.
Li, C., Zhang, J., Hu, G., Fu, Y., Wang, Q., 2016a. Association mapping and favorable allele mining for node of first fruiting/sympodial branch and its height in upland cotton (Gossypium hirsutum L.). Euphytica 210, 57-68.
Li, C.Q., Guo, W.Z., Ma, X.L., Zhang, T.Z., 2008. Tagging and mapping of QTL for yield and its components in upland cotton (Gossypium hirsutum L.) population with varied lint percentage. Acta Gossypii Sinica 20, 163-169.
Li, C.Q., Xu, X.J., Dong, N., Ai, N.J., Wang, Q.L., 2016b. Association mapping identifies markers related to major early-maturating traits in upland cotton (Gossypium hirsutumL.). Plant Breed. 135, 483-491.
Liu, G.Z., Mei, H.X., Wang, S., Li, X.H., Zhu, X.F., Zhang, T.Z., 2015. Association mapping of seed oil and protein contents in upland cotton. Euphytica 205, 637-645.
May, O.L., Bowman, D.T., Calhoun, D.S., 1995. Genetic diversity of U.S. upland cotton cultivars released between 1980 and 1990. Crop Sci. 35, 1570-1574.
Mei, H.X., Ai, N.J., Zhang, X., Ning, Z.Y., Zhang, T.Z., 2014. QTLs conferring FOV 7 resistance detected by linkage and association mapping in upland cotton. Euphytica 197, 237-249.
Mei, H.X., Zhu, X.F., Zhang, T.Z., 2013. Favorable QTL alleles for yield and its components identified by association mapping in Chinese upland cotton cultivars. PloS One 8, e82193.
Nie, X.H., Huang, H., You, C.Y., Li, W., Zhao, W.X., Shen, C., Zhang, B.B., Wang, H.T., Yan, Z.H., Dai, B.S., Wang, M.J., Zhang, X.L., Lin, Z.X., 2016. Genome-wide SSRbased association mapping for fiber quality in nation-wide upland cotton inbreed cultivars in China. BMC Genom. 17, 352.
Peakall, R., Smouse, P.E., 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537-2539.
Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945-959.
Qin, H.D., Chen, M., Yi, X.D., Bie, S., Zhang, C., Zhang, Y.C., Lan, J.Y., Meng, Y.Y., Yuan, Y.L., Jiao, C.H., 2015. Identification of associated SSR markers for yield component and fiber quality traits based on frame map and Upland cotton collections. PloS One 10, e0118073.
Rungis, D., Llewellyn, D., Dennis, E.S., Lyon, B.R., 2005. Simple sequence repeat (SSR) markers reveal low levels of polymorphism between cotton (Gossypium hirsutum L.) cultivars. Aust. J. Agric. Res. 56, 301-307.
Shappley, Z.W., Jenkins, J., Zhu, J., McCarty Jr., J.C., 1998. Quantitative trait loci associated with agronomic and fiber traits of upland cotton. J. Cotton Sci. 2, 153-163.
Shen, X.L., Guo, W.Z., Lu, Q.X., Zhu, X.F., Yuan, Y.L., Zhang, T.Z., 2007. Genetic mapping of quantitative trait loci for fiber quality and yield trait by RIL approach in Upland cotton. Euphytica 155, 371-380.
Shen, X.L., Guo, W.Z., Zhu, X.F., Yuan, Y.L., Yu, J.Z., Kohel, R.J., Zhang, T.Z., 2005. Molecular mapping of QTLs for fiber qualities in three diverse lines in Upland cotton using SSR markers. Mol. Breed. 15, 169-181.
Song, M.Z., Yu, S.X., Fan, S.L., Ruan, R.H., Huang, Z.M., 2005. Genetic analysis of main agronomic traits in short season upland cotton. Acta Gossypii Sinica 17, 94-98.
Stephens, S.G., 1958. Salt water tolerance of seeds of Gossypium species as a possible factor in seed dispersal. Am. Nat. 92, 83-92.
Thornsberry, J.M., Goodman, M.M., Doebley, J., Kresovich, S., Nielsen, D., Buckler, E.S., 2001. Dwarf 8 polymorphisms associate with variation in flowering time. Nat. Genet. 28, 286-289.
Tyagi, P., Gore, M.A., Bowman, D.T., Campbell, B.T., Udall, J.A., Kuraparthy, V., 2014. Genetic diversity and population structure in the US upland cotton (Gossypium hirsutum L.). Theor. Appl. Genet. 127, 283-295.
Ulloa, M., Meredith Jr., W.R., 2000. Genetic linkage map and QTL analysis of agronomic and fiber quality traits in an intraspecifc population. J. Cotton Sci. 4, 161-170.
Wang, B.H., Draye, X., Zhuang, Z.M., Zhang, Z.S., Liu, M., Lubbers, E.L., Jones, D., May, O.L., Paterson, A.H., Chee, P.W., 2017a. QTL analysis of cotton fiber length in advanced backcross populations derived from a cross between Gossypium hirsutum and G. mustelinum. Theor. Appl. Genet. 130, 1297-1308.
Wang, B.H., Guo, W.Z., Zhu, X.F., Wu, Y.T., Huang, N.T., Zhang, T.Z., 2006. QTL mapping of fiber quality in an elite hybrid derived-RIL population of upland cotton. Euphytica 152, 367-378.
Wang, K.B., Wang, Z.W., Li, F.G., Ye, W.W., Wang, J.Y., Song, G.L., Yue, Z., Cong, L., Shang, H.H., Zhu, S.L., Zou, C.S., Li, Q., Yuan, Y.L., Lu, C.R., Wei, H.L., Gou, C.Y., Zheng, Z.Q., Yin, Y., Zhang, X.Y., Liu, K., Wang, B., Song, C., Shi, N., Kohel, R.J., Percy, R.G., Yu, J.Z., Zhu, Y.X., Wang, J., Yu, S.X., 2012. The draft genome of a diploid cotton Gossypium raimondii. Nat. Genet. 44, 1098-1103.
Wang, L., Wu, S.M., Zhu, Y., Fan, Q., Zhang, Z.N., Hu, G., Peng, Q.Z., Wu, J.H., 2017b. Functional characterization of a novel jasmonate ZIM-domain interactor (NINJA) from upland cotton (Gossypium hirsutum). Plant Physiol. Biochem. 112, 152-160.
Wen, T.W., Wu, M., Shen, C., Gao, B., Zhu, D., Zhang, X.L., You, C.Y., Lin, Z.X., 2018. Linkage and association mapping reveals the genetic basis of brown fiber(Gossypium hirsutum). Plant Biotechnol. J. 16, 1654-1666.
Wendel, J.F., Brubaker, C., Alvarez, I., Cronn, R., Stewart, J.M., 2009. Evolution and natural history of the cotton genus. In: Paterson, A.H. (Ed.), Genetics and Genomics of Cotton. Springer., New York, pp. 3-22.
Wendel, J.F., Brubaker, C.L., Percival, A.E., 1992. Genetic diversity in Gossypium hirsutum and the origin of upland cotton. Am. J. Bot. 79, 1291-1310.
Wendel, J.F., Cronn, R.C., 2003. Polyploidy and the evolutionary history of cotton. Adv. Agron. 78, 139-186.
Xu, Q.H., Zhang, X.L., Nie, Y.C., 2001. Genetic diversity evaluation of cultivars(G. hirsutum L.) from the Changjiang river valley and Yellow river valley by RAPD markers. Acta Genetica Sin. 28, 683-690.
Yeh, F., Boyle, T.J.B., 1996. Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belg. J. Bot. 129, 157.
Yu, J.M., Pressoir, G., Briggs, W.H., Bi, I.V., Yamasaki, M., Doebley, J.F., McMullen, M.D., Gaut, B.S., Nielsen, D.M., Holland, J.B., Kresovich, S., Buckler, E.S., 2006. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203-208.
Zeng, L.H., Meredith Jr., W.R., Gutiérrez, O.A., Boykin, D.L., 2009. Identi fication of associations between SSR markers and fiber traits in an exotic germplasm derived from multiple crosses among Gossypium tetraploid species. Theor. Appl. Genet. 119, 93-103.
Zhang, J.F., Lu, Y.Z., Cantrell, R., Hughs, S.E., 2005. Molecular marker diversity and field performance in commercial cotton cultivars evaluated in the Southwestern USA. Crop Sci. 45, 1483-1490.
Zhao, Y.L., Wang, H.M., Chen, W., Li, Y.H., 2014. Genetic structure, linkage disequilibrium and association mapping of verticillium wilt-resistance in elite cotton(Gossypium hirsutum L.) germplasm population. PloS One 9, e86308.
Zhu, C.S., Gore, M., Buckler, E.S., Yu, J.M., 2008. Status and prospects of association mapping in plants. Plant Genome 1, 5-20.

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