Research Paper

Potential of sweet potato (Ipomoea batatas (L.) Lam.) breeding populations evaluated based on expressed sequence tags-simple sequence repeats

Kuan-Hung Lin, Yu-Wen Chang, Yung-Chang Lai, Shih-Ying Hwang

Published on: 26 July 2023

Page: 303 - 313

DOI: 10.6165/tai.2023.68.303

Abstract

Expressed sequence tags-derived simple sequence repeats (EST-SSRs) are related to functional genes and can be useful in crop breeding. Parental lines selected in sweet potato (Ipomoea batatas (L.) Lam.) breeding including controlled hybridization and polycross may be originated from a limited number of genetic sources. We surveyed genetic variation of three breeding populations (hybrid, landrace, and polycross) of 89 cultivated sweet potato varieties derived from controlled hybridization (41 hybrids) and polycross (38 varieties) breeding population and landrace (10 varieties) maintained by various geographic regions and main agronomic traits of local farmers, using 23 EST-SSRs. Six wild sweet potato (I. trifida) samples were also included in the study. High genetic diversity in the three types of breeding populations was detected. High proportions of shared alleles leading to low levels of differentiation between breeding populations were discovered. The neighbor-joining tree and individual assignments showed intermingling of varieties among the three breeding populations. Additionally, genetic clustering showed little power of grouping varieties of different breeding populations into separate clades. These results indicate limits of sweet potato breeding. Nevertheless, ten alleles of nine loci showed variance contributed significantly to the delimitation of varieties in different breeding populations.

Keyword: Breeding, EST, Ipomoea batatas, markers, SSR, sweet potato

Literature Cited

Adamack, A.T., Gruber, B. 2014 PopGenReport: simplifying basic population genetic analyses in R. Methods Ecol. Evol. 5(4): 384?387.
DOI: 10.1111/2041-210X.12158View Article Google Scholar

Agapow, P.M., Burt, A. 2001 Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1(1-2): 101–102.
DOI: 10.1046/j.1471-8278.2000.00014.xView Article Google Scholar

Aggarwal, R.K., Hendre, P.S., Varshney, R.K., Bhat, P.R., Krishnakumar, V., Singh, L. 2007 Identification, characterization, and utilization of EST-derived genic microsatellite makers for genome analyses of coffee and related species. Theor. Appl. Genet. 114(2): 359?372.
DOI: 10.1007/s00122-006-0440-xView Article Google Scholar

Allard, R.W. 1970 Population structure and sampling methods. In: Frankel, O.H., Bennett, E. (Eds.) Genetic Resources in Plants – Their Exploration and Conservation 97–107pp. Blackwell Scientific Publications, Oxford.

Andersen, J. R., L?bberstedt, T. 2003 Functional markers in plants. Trends Plant Sci. 8(11): 554?560.
DOI: 10.1016/j.tplants.2003.09.010View Article Google Scholar

Archer, F.I., Adams, P.E., Schneiders, B.B. 2017 strataG: An R package for manipulating, summarizing and analysing population genetic data. Mol. Ecol. Resour. 17(1): 5–11.
DOI: 10.1111/1755-0998.12559View Article Google Scholar

Bates, D., Maechler, M., Bolker, B., Walker, S. 2015 Fitting linear mixed-effects models using lme4. J. Stat. Soft. 67(1): 1–48.
DOI: 10.18637/jss.v067.i01View Article Google Scholar

Bhandari, H.R. Bhanu, A.N., Srivastava, K., Singh,.M.N., Shreya, Hemantaranjan, A. 2017 Assessment of genetic diversity in crop plants – an overview. Adv. Plants Agricul. Res. 7(3): 279?286.
DOI: 10.15406/apar.2017.07.00255View Article Google Scholar

Brown, A. H., Feldman, M. W., Nevo, E. 1980 Multilocus structure of natural populations of Hordeum spontaneum. Genetics 96(2): 523–536.
DOI: 10.1093/genetics/96.2.523View Article Google Scholar

Buckler, E.S., Thornsberry J.M. 2002 Plant molecular diversity and applications to genomics. Curr. Opin. Plant Biol. 5(2):107–111.
DOI: 10.1016/S1369-5266(02)00238-8View Article Google Scholar

Ceccarelli, S., Grando, S., Maatougui, M., Micheal, M., Slash, M., Haghparast, R., Rahmanian, M., Taheri, A., Al-Yassin, A., Benbelkacem, A., Labdi, M., Mimoun, H., Nachit, M. 2010 Plant breeding and climate changes. J. Agricul. Sci. 148(6): 627?637.

Ceccarelli, S., Grando, S. 2020 Evolutionary plant breeding as a response to the complexity of climate change. iScience 23(12):101815.
DOI: 10.1016/j.isci.2020.101815View Article Google Scholar

Chapman, M.A., Pashley, C.H., Wenzler, J., Hvala, J., Tang, S., Knapp, S,J., Burke, J,M. 2008 A genomic scan for selection reveals candidates for genes involved in the evolution of cultivated sunflower (Helianthus annuus). Plant Cell 20(11): 2931?2945.
DOI: 10.1105/tpc.108.059808View Article Google Scholar

Cortinovis, G., Di Vittori, V., Bellucci, E., Bitocchi, E., Papa, R. 2020 Adaptation to novel environments during crop diversification. Curr. Opin. Plant Biol. 56: 203?217.
DOI: 10.1016/j.pbi.2019.12.011View Article Google Scholar

Collard, B.C.Y., Mackill, D.J. 2008. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Phil. Trans. R. Soc. B 363(1491):557?572.
DOI: 10.1098/rstb.2007.2170View Article Google Scholar

Da Silva, J.A., Solis-Gracia, N. 2006. Development of simple sequence repeat markers from genes related to stress resistance in sugarcane. Subtropical Plant Sci. 58: 5?11.

Dillon, S. L., Shapter, F.M., Henry, R.J., Cordeiro, G., Izquierdo, L., Lee, L.S. 2007 Domestication to crop improvement: genetic resources for Sorghum and Saccharum (Andropogoneae). Ann. Bot. 100(5): 975?989.
DOI: 10.1093/aob/mcm192View Article Google Scholar

Doyle, J.J., Doyle, J.L. 1987 A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem. Bull. 19: 11–15.

Dray, S., Dufour, A.B. 2007 The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22(4): 1–20.
DOI: 10.18637/jss.v022.i04View Article Google Scholar

Elameen, A., Fjellheim, S., Larsen, A., Rognli, O.A., Sundheim, L., Msolla, S., Masumba, E., Mtunda, K., Klemsdal, S.S. 2008 Analysis of genetic diversity in a sweet potato (Ipomoea batatas L.) germplasm collection from Tanzania as revealed by AFLP. Genet. Resour. Crop Evol. 55(3): 397–408.
DOI: 10.1007/s10722-007-9247-0View Article Google Scholar

Elshafei, A.A., Afiah, S.A.E.-A., Al-Doss, A.A., Ibrahim, E.I. 2019 Morphological variability and genetic diversity of wheat genotypes grown on saline soil and identification of new promising molecular markers associated with salinity tolerance. Int. J. Plant Inter. 14(1): 564?571.
DOI: 10.1080/17429145.2019.1672815View Article Google Scholar

Ercan, S. Ertugrul, F., Aydin, Y., Akfirat, F.S., Hasancebi, S., Akan, K., Mert, Z., Bolat, N., Yorgancilar, O., Altinkut-Uncuoglu, A. 2010 An EST-SSR marker linked with yellow rust resistance in wheat. Biol. Planta 54(4): 691?696.
DOI: 10.1007/s10535-010-0122-zView Article Google Scholar

Ersoz, E.S., Yu, J., Buckler, E.S. 2007 Applications of linkage disequilibrium and association mapping in crop plants. In: Varshney, R.K., Tuberosa, R. (eds) Genomics-Associated Crop Improvement Vol. 1: Genomics Approaches and Platforms 97–107pp. Springer, The Netherlands.
DOI: 10.1007/978-1-4020-6295-7_5View Article Google Scholar

Eujayl, I., Sorrells, M.E., Baum, M., Wolters, P., Powell, W. 2002 Isolation of EST-derived microsatellite markers of phenotyping the A and B genomes of wheat. Theor. Appl. Genet. 104(2): 399?407.
DOI: 10.1007/s001220100738View Article Google Scholar

Fox, J., Weisberg, S. 2011 An R companion to applied regression, 2nd Edn. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion (Sage, 2011).

Frichot, E., Fran?ois, O. 2015 LEA: an R package for landscape and ecological association studies. Methods Ecol. Evol. 6(8): 925–929.
DOI: 10.1111/2041-210X.12382View Article Google Scholar

Gao, M., Soriano, S.F., Cao, Q., Yang X., Lu, G. 2020 Hexaploid sweetpotato (Ipomoea batatas (L.) Lam.) may not be a true type to either auto- or allopolyploid. PLoS One 15(3): e0229624.
DOI: 10.1371/journal.pone.0229624View Article Google Scholar

Gemenet, D.C., Kitavi, M.N., David, M., Ndege, D., Ssali, R.T., Swanckaert, J., Makunde, G., Yencho, G.C., Gruneberg, W., Carey, E., Mwanga, R.O., Andrade, M.I., Heck, S., Campos, H., Kumar, A. 2019 Development of diagnostic SNP markers for quality assurance and control in sweetpotato [Ipomoea batatas (L.) Lam.] breeding Programs. PLoS One 15(4): e0232173.
DOI: 10.1371/journal.pone.0232173View Article Google Scholar

Gupta, D.S., Cheng, P., Sablok, G., Thavarajah, D., Thavarajah, P., Coyne, C.J., Kumar, S., Baum, M., McGee, R.J. 2016 Development of a panel of unigene-derived polymorphic EST-SSR markers in lentil using public database information. The Crop J. 4(5): 425?433.
DOI: 10.1016/j.cj.2016.06.012View Article Google Scholar

Guo, S.W., Thompson, E.A. 1992 Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48(2): 361–372.
DOI: 10.2307/2532296View Article Google Scholar

Goudet, J., Jombart, T. 2020 hierfstat: Estimation and Tests of Hierarchical F-Statistics. R package version 0.5-7. https://CRAN.R-project.org/package=hierfstat.

Gwandu, C., Tairo, F., Mneney, E., Kullaya, A. 2012 Characterization of Tanzanian elite sweet potato genotypes for sweet potato virus disease (SPVD) resistance and high dry matter content using simple sequence repeat (SSR) markers. Afr. J. Biotechnol. 11(40): 9582–9590.
DOI: 10.5897/AJB11.4208View Article Google Scholar

Hu, J.J., Nakatani, M., Mizuno, K., Fujimura, T. 2004a Development and characterization of microsatellite markers in sweetpotato. Breed. Sci. 54(2): 177?188.
DOI: 10.1270/jsbbs.54.177View Article Google Scholar

Hu, J.J., Nakatani, M., Lalusin, A. G., Fujimura, T. 2004b New microsatellite markers developed from reported Ipomoea trifida sequences and their application to sweet potato and its related wild species. Sci. Horticul. 102(4): 375–386.
DOI: 10.1016/j.scienta.2004.04.014View Article Google Scholar

Hwang, S.Y., Tseng, Y.T., Lo, H.F. 2002 Application of simple sequence repeats in determining the genetic relationships of varieties used in sweet potato polycross breeding in Taiwan. Sci. Horticul. 93(3-4): 215?224.
DOI: 10.1016/S0304-4238(01)00343-0View Article Google Scholar

Isabel, L. P., Park, J.R., Lee, G. S., Park, G.H., Kim, K.M. 2019 Development of EST-SSR markers and analysis of genetic relationship it’s resources in hexaploidy oats. J. Crop Sci. Biotech. 22(3): 243?251.
DOI: 10.1007/s12892-019-0158-0View Article Google Scholar

Jombart, T., Devillard, S., Balloux, F. 2010 Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11(1): 94.
DOI: 10.1186/1471-2156-11-94View Article Google Scholar

Jombart, T., Ahmed, I. 2011 adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27(21): 3070–3071.
DOI: 10.1093/bioinformatics/btr521View Article Google Scholar

Jones, A. 1965 A proposed breeding procedure for sweet potato. Crop Sci. 5(2):191?192.
DOI: 10.2135/cropsci1965.0011183X000500020033xView Article Google Scholar

Kamvar, Z. N., Brooks, J. C., Gr?nwald, N. J. 2015. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6: 208.
DOI: 10.3389/fgene.2015.00208View Article Google Scholar

Keneni, G., Bekele, E., Imtiaz, M., Dagne, K. 2012. Genetic vulnerability of modern crop varieties: causes, mechanism and remedies. Int. J. Plant Res. 2(3): 69?79 .
DOI: 10.5923/j.plant.20120203.05View Article Google Scholar

Kim, J.H., Jo, W.A., Ham J.G., Chung, K., Kim, K.M. 2016 Characterization and development of EST-SSR markers in sweet potato (Ipomoea batatas (L.) Lam). 3 Biotech. 6(2): 243.
DOI: 10.1007/s13205-016-0565-9View Article Google Scholar

Kota, R., Varshney, R.K., Thiel, T., Dehmer, K.J., Graner, A. 2001 Generation and comparison of EST-derived SSRs and SNPs in barley (Hordeum vulgare L.). Hereditas 135(2-3): 145?151.
DOI: 10.1111/j.1601-5223.2001.00145.xView Article Google Scholar

Kriegner, A., Cervantes, J.C., Burg, K., Mwanga, R.O.M., Zhang, D. 2003 A genetic linkage map of sweetpotato [Ipomoea batatas (L.) Lam.] based on AFLP markers. Mol. Breed. 11: 169–185.

Lavergne, S., Molofsky, J. 2007 Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc. Natl. Acad. Sci. USA 104(10): 3883?3888.
DOI: 10.1073/pnas.0607324104View Article Google Scholar

Lenth, R. 2020 emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.8. https://CRAN.R-project.org/package=emmeans.

Louwaars, N.P. 2018 Plant breeding and diversity: A troubled relationship? Euphytica 214(7): 114.
DOI: 10.1007/s10681-018-2192-5View Article Google Scholar

Ma, J., Chen, J., Zhang, C., Yang, D., Tang, W., Gao, F., Xie, Y., Sun, H. 2022 Development and characterisation of SSR markers in the potato rot nematode Ditylenchus destructor Nematology 24(9): 959–969.
DOI: 10.1163/15685411-bja10183View Article Google Scholar

Marshall, D. R., Brown, A. H. D. 1975 Optimum sampling strategies in genetic conservation. In: Frankel, O.H., Hawks, J.G. (eds) Crop Genetic Resources for Today and Tomorrow 53?80pp. Cambridge University Press, Cambridge.

Meng, Y., Zheng, C., Li, H., Li, A., Zhai, H., Wang, Q., He, S., Zhao, N., Zhang, H., Gao, S., Liu, Q. 2021 Development of a high-density SSR genetic linkage map in sweet potato. Crop J. 9(6): 1367–1374
DOI: 10.1016/j.cj.2021.01.003View Article Google Scholar

Mu?oz-Rodr?guez, P., Carruthers, T., Wood, J.R.I., Williams, B.R.M., Weitemier, K., Kronmiller, B., Ellis, D., Anglin, N.L., Longway, L., Harris, S.A., Rausher, M.D., Kelly, S., Liston, A., Scotland, R.W. 2018 Reconciling conflicting phylogenies in the origin of sweet potato and dispersal to Polynesia. Curr. Biol. 28(8): 1246–1256.
DOI: 10.1016/j.cub.2018.03.020View Article Google Scholar

Nei, M. 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89(3): 583–590.
DOI: 10.1093/genetics/89.3.583View Article Google Scholar

Ngailo, S., Shimelis, H., Sibiya, J., Amelework, B., Mtunda, K. 2016 Genetic diversity assessment of Tanzanian sweetpotato genotypes using simple sequence repeat markers. South Afr. J. Bot. 102: 40?45.
DOI: 10.1016/j.sajb.2015.08.001View Article Google Scholar

Nishiyama, I., Miyazaki, T., Sakamoto, S. 1975 Evolutionary autoploid in the sweet potato (Ipomoea batatas (L.) Lam.) and its progenitors. Euphytica 24(1): 197?208.
DOI: 10.1007/BF00147186View Article Google Scholar

Paradis, E., Schliep, K. 2019 ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35(3): 526–528.
DOI: 10.1093/bioinformatics/bty633View Article Google Scholar

Qiu, L., Yang, C., Tian, B., Yang, J.B., Liu, A. 2010 Exploiting EST databases for the development and characterization of EST-SSR markers in castor bean (Ricinus communis L.). BMC Plant Biol. 10(1): 278.
DOI: 10.1186/1471-2229-10-278View Article Google Scholar

Quain, M.D., Adofo, K., Appiah-Kubi, D., Prempeh, R.N., Asafu-Agyei, J., Akomeah, B., Dapaah, H. 2018 Use of expressed sequence tags-derived simple sequence repeat (SSR) markers for population studies of released and elite sweet potato. Int. J. Genet. Mol. Bio. 10(2):14?25.
DOI: 10.5897/IJGMB2017.0159View Article Google Scholar

Slatkin, M. 1993 Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47(1): 264–279.
DOI: 10.2307/2410134View Article Google Scholar

Rodriguez-Bonilla, L., Cuevas, H.E., Montero-Rojas, M., Bird-Pico, F., Luciano-Rosario, D., Siritunga, D., Nelson, M.N. 2014 Assessment of genetic diversity of sweet potato in Puerto Rico. PLoS One 9(12): e116184.
DOI: 10.1371/journal.pone.0116184View Article Google Scholar

Roullier, C., Duputi?, A., Wennekes, P., Benoit, L., Bringas, V.M.F., Rossel, G., Tay, D., McKey, D., Lebot, V., Joly, S. 2013a Disentangling the origins of cultivated sweet potato (Ipomoea batatas (L.) Lam.). PLoS One 8(5): e62707.
DOI: 10.1371/annotation/936fe9b4-41cb-494d-87a3-a6d9a37c6c68View Article Google Scholar

Roullier, C., Kambouo, R., Paofa, J., McKey, D.B., Lebot, V. 2013b On the origin of sweet potato (Ipomoea batatas (L.) Lam.) genetic diversity in New Guinea, a secondary center of diversity. Heredity 110(6): 594–604.
DOI: 10.1038/hdy.2013.14View Article Google Scholar

Rousset, F. 2008 genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resour. 8(1): 103?106 .
DOI: 10.1111/j.1471-8286.2007.01931.xView Article Google Scholar

Thiel, T., Michalek, W., Varshney, R.K., Graner, A. 2003 Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor. Appl. Genet. 106(3): 411?422 .
DOI: 10.1007/s00122-002-1031-0View Article Google Scholar

Ting, C.Y., Kehr, E.A. 1953 Meiotic studies in the sweet potato (Ipomoea batatas Lam.). J. Hered. 34: 207?211.

Tseng, Y.T., Lo, H.F., Hwang, S.Y. 2002 Genotyping and assessment of genetic relationships in elite polycross breeding varieties of sweet potato in Taiwan based on SAMPL polymorphisms. Bot. Bull. Acad. Sin. 43(2): 99?105.
DOI: 10.7016/BBAS.200204.0099View Article Google Scholar

Tumwegamire, S., Rubaihayo, P.R., LaBonte, D.R., Diaz, F., Kapinga, R., Mwanga, R.O.M., Gruneberg, W.J. 2011 Genetic diversity in white- and orange-fleshed sweet potato farmer varieties from east Africa evaluated by simple sequence repeat markers. Crop Sci. 51(3):1132–1142.
DOI: 10.2135/cropsci2010.07.0407View Article Google Scholar

Varshney, R. K., Graner, A., Sorrells, M. E. 2005a Genetic microsatellite markers in plants: features and applications. Trends Biotechnol. 23(1): 48?55.
DOI: 10.1016/j.tibtech.2004.11.005View Article Google Scholar

Varshney, R.K., Prasad, M., Kota, R., Sigmund, R., Valkoun, B?rner, A., Valkoun, J., Scholz, U., Stein, N., Graner, A. 2005b Functional molecular markers in barley: Development and applications. Czech J. Genet. Plant Breed. 41(10): 128?133.
DOI: 10.17221/6152-CJGPBView Article Google Scholar

Wadl, P.A., Olukolu, B.A., Branham, S.E., Jarret, R.L., Yencho, G.C., Jackson, D.M. 2018 Genetic diversity and population structure of the USDA sweetpotato (Ipomoea batatas) germplasm collections using GBSpoly. Front. Plant Sci. 9: 1166.
DOI: 10.3389/fpls.2018.01166View Article Google Scholar

Wang, Z., Li, J., Luo, Z., Huang, L., Chen, X., Fang, B., Li, Y., Chen, J., Zhang, X. 2011 Characterization and development of EST-derived SSR markers in cultivated sweetpotato (Ipomoea batatas). BMC Plant Biol. 11(1):139.
DOI: 10.1186/1471-2229-11-139View Article Google Scholar

Yada, B., Tukamuhabwa, P., Wanjala, B., Kim, D.-J., Skilton, R.A., Alajo, A., Mwanga, R.O.M. 2010 Characterizing Ugandan sweet potato germplasm using fluorescent labeled simple sequence repeat markers. Hort. Sci. 45(2): 225–230.
DOI: 10.21273/HORTSCI.45.2.225View Article Google Scholar

Yu, Y., Yuan, D., Liang, S., Li, X., Wang, X., Lin, Z., Zhang, X. 2011 Genome structure of cotton revealed by a genome-wide SSR genetic map constructed from a BC1 population between Gossypium hirsutum and G. barbadense. BMC Genom. 12(1): 15.
DOI: 10.1186/1471-2164-12-15View Article Google Scholar

Zhu, Q., Zheng, X., Luo, J., Gaut, B. S., Ge, S. 2007. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol. Biol. Evol. 24(3): 857?888.
DOI: 10.1093/molbev/msm005View Article Google Scholar