Genetic variation developed in plant breeding
programs is fundamental to creating new combinations that result in cultivars
with enhanced characteristics. Over the years, tomato (Solanum lycopersicum) breeding programs associated with the Texas A&M
University system have developed morphologically diverse lines of tomatoes
selected for heat tolerance, fruit quality, and disease resistance to adapt
them to Texas growing conditions. Here we explored the intraspecific genetic
variations of 322 cultivated tomato genotypes, including 300 breeding lines
developed by three Texas A&M breeding programs, as an initial step toward
implementing molecular breeding approaches. Genotyping by sequencing using low
coverage whole-genome sequencing (SkimGBS) identified 10,236 high-quality
single-nucleotide polymorphisms (SNPs) that were used to assess genetic
diversity, population structure, and phylogenetic relationship between
genotypes and breeding programs. Model-based population structure analysis,
phylogenetic tree construction, and principal component analysis indicated that
the genotypes were grouped into two main clusters. Genetic distance analysis
revealed greater genetic diversity？ among
the products of the three breeding programs. The germplasm developed at Texas A&M
programs at Weslaco, College Station, and by Dr. Paul Leeper exhibited genetic
diversity ranges of 0.175 - 0.434, 0.099 - 0.392, and 0.183 - 0.347, respectively,
suggesting that there is enough variation within and between the lines from the
three programs to perform selection for cultivar development. The SNPs
identified here could be used to develop molecular tools for selecting various
traits of interest and to select parents for future tomato breeding.
References
[1]
Foolad, M.R. (2007) Genome Mapping and Molecular Breeding of Tomato. International Journal of Plant Genomics, 2007, Article ID: 64358.
https://doi.org/10.1155/2007/64358
[2]
Menda, N., Strickler, S.R. and Mueller, L.A. (2013) Advances in Tomato Research in the Post-Genome Era. Plant Biotechnology, 30, 243-256.
https://doi.org/10.5511/plantbiotechnology.13.0904a
[3]
Rothan, C., Diouf, I. and Causse, M. (2019) Trait Discovery and Editing in Tomato. Plant Journal, 97, 73-90. https://doi.org/10.1111/tpj.14152
[4]
National Agricultural Statistics Service (2018) Vegetables 2018 Summary. United States Department of Agriculture, Washington DC.
[5]
National Agricultural Statistics Service (2017) Census of Agriculture. United States Department of Agriculture, Washington DC.
[6]
Texas Department of Agriculture (2014) Production versus Consumption Surplus and Deficit. Texas Agricultural Commodities.
[7]
Segovia-Coronel, M. (2014) Measuring Consumer Acceptance and Willingness to Pay for Specialty Tomatoes: Impact of Product Taste and Health Features. Department of Agricultural Economics, Texas A & M, College Station.
[8]
Lee, J.H.J., Jayaprakasha, G.K., Avila, C.A., Crosby, K.M. and Patil, B.S. (2019) Metabolomic Studies of Volatiles from Tomatoes Grown in Net-House and Open-Field Conditions. Food Chemistry, 275, 282-291.
https://doi.org/10.1016/j.foodchem.2018.09.091
[9]
Lazarte, J.E., Leeper, P.W. and Barringer, R.K. (1981) High-Temperature Fruit Set of Tomatoes. HortScience, 16, 289-289.
Lazarte, J.E., Leeper, P.W. and Barringer, R.K. (1981) High-Temperature Effects on Tomato Fruit-SET. HortScience, 16, 444-445.
[12]
Leeper, P.W. (1969) TAMU “Chico III”: A Pear Type, Disease Resistant Tomato Designed for Machine Harvest. T.A.M.U. Texas Agricultural Experimental Station, College Station.
[13]
Acquaah, G. (2012) Variation: Types, Origin and Scale. In: Principles of Plant Genetics and Breeding, 2nd Edition, John Wiley & Sons, Ltd., Hoboken.
[14]
Bisen, A., Khare, D., Nair, P. and Tripathi, N. (2015) SSR Analysis of 38 Genotypes of Soybean (Glycine max (L.) Merr.) Genetic Diversity in India. Physiology and Molecular Biology of Plants, 21, 109-115.
https://doi.org/10.1007/s12298-014-0269-8
[15]
Denwar, N.N., Awuku, F.J., Diers, B., Addae-Frimpomaah, F., Chigeza, G., Oteng-Frimpong, R., Puozaa, D.K. and Barnor, M.T. (2019) Genetic Diversity, Population Structure and Key Phenotypic Traits Driving Variation within Soybean (Glycine max) Collection in Ghana. Plant Breeding.
https://doi.org/10.1111/pbr.12700
[16]
Miller, J.C. and Tanksley, S.D. (1990) RFLP Analysis of Phylogenetic Relationships and Genetic Variation in the Genus Lycopersicon. Theoretical and Applied Genetics, 80, 437-448. https://doi.org/10.1007/BF00226743
[17]
Zhao, J.T., Xu, Y., Ding, Q., Huang, X.L., Zhang, Y.T., Zou, Z.R., Li, M., Cui, L. and Zhang, J. (2016) Association Mapping of Main Tomato Fruit Sugars and Organic Acids. Frontiers in Plant Science, 7, 1286. https://doi.org/10.3389/fpls.2016.01286
[18]
Sacco, A., Ruggieri, V., Parisi, M., Festa, G., Rigano, M. M., Picarella, M.E., Mazzucato, A. and Barone, A. (2015) Exploring a Tomato Landraces Collection for Fruit-Related Traits by the Aid of a High-Throughput Genomic Platform. PLoS ONE, 10, e0137139. https://doi.org/10.1371/journal.pone.0137139
[19]
Lin, T., Zhu, G.T., Zhang, J.H., Xu, X.Y., Yu, Q.H., Zheng, Z., Zhang, Z.H., Lun, Y.Y., Li, S., Wang, X.X., Huang, Z.J., Li, J.M., Zhang, C.Z., Wang, T.T., Zhang, Y.Y., Wang, A.X., Zhang, Y.C., Lin, K., Li, C.Y., Xiong, G.S., Xue, Y.B., Mazzucato, A., Causse, M., Fei, Z.J., Giovannoni, J.J., Chetelat, R.T., Zamir, D., Stadler, T., Li, J.F., Ye, Z.B., Du, Y.C. and Huang, S.W. ( 2014) Genomic Analyses Provide Insights into the History of Tomato Breeding. Nature Genetics, 46, 1220-1226.
https://doi.org/10.1038/ng.3117
[20]
Aflitos, S., Schijlen, E., de Jong, H., de Ridder, D., Smit, S., Finkers, R., Wang, J., Zhang, G., Li, N., Mao, L., Bakker, F., Dirks, R., Breit, T., Gravendeel, B., Huits, H., Struss, D., Swanson-Wagner, R., van Leeuwen, H., van Ham, R.C., Fito, L., Guignier, L., Sevilla, M., Ellul, P., Ganko, E., Kapur, A., Reclus, E., de Geus, B., van de Geest, H., Lintel Hekkert, B.T., van Haarst, J., Smits, L., Koops, A., Sanchez-Perez, G., van Heusden, A.W., Visser, R., Quan, Z., Min, J., Liao, L., Wang, X., Wang, G., Yue, Z., Yang, X., Xu, N., Schranz, E., Smets, E., Vos, R., Rauwerda, J., Ursem, R., Schuit, C., Kerns, M., van den Berg, J., Vriezen, W., Janssen, A., Datema, E., Jahrman, T., Moquet, F., Bonnet, J. and Peters, S. (2014) Exploring Genetic Variation in the Tomato (Solanum Section Lycopersicon) Clade by Whole-Genome Sequencing. Plant Journal, 80, 136-148. https://doi.org/10.1111/tpj.12616
[21]
Phan, N.T., Trinh, L.T., Rho, M.Y., Park, T.S., Kim, O.R., Zhao, J., Kim, H.M. and Sim, S.C. (2019) Identification of Loci Associated with Fruit Traits Using Genome-Wide Single Nucleotide Polymorphisms in a Core Collection of Tomato (Solanum lycopersicum L.). Scientia Horticulturae, 243, 567-574.
https://doi.org/10.1016/j.scienta.2018.09.003
[22]
Ruggieri, V., Francese, G., Sacco, A., D’Alessandro, A., Rigano, M.M., Parisi, M., Milone, M., Cardi, T., Mennella, G. and Barone, A. (2014) An Association Mapping Approach to Identify Favourable Alleles for Tomato Fruit Quality Breeding. BMC Plant Biology, 14, 337. https://doi.org/10.1186/s12870-014-0337-9
[23]
The Tomato Genome Consortium (2012) The Tomato Genome Sequence Provides Insights into Fleshy Fruit Evolution. Nature, 485, 635-641.
https://doi.org/10.1038/nature11119
[24]
Chung, Y.S., Choi, S.C., Jun, T.H. and Kim, C. (2017) Genotyping by Sequencing: A Promising Tool for Plant Genetics Research and Breeding. Horticulture Environment and Biotechnology, 58, 425-431. https://doi.org/10.1007/s13580-017-0297-8
[25]
Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S. and Mitchell, S.E. (2011) A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. PLoS ONE, 6, e19379.
https://doi.org/10.1371/journal.pone.0019379
[26]
Labate, J.A., Sheffer, S.M., Balch, T. and Robertson, L.D. (2011) Diversity and Population Structure in a Geographic Sample of Tomato Accessions. Crop Science, 51, 1068-1079. https://doi.org/10.2135/cropsci2010.05.0305
[27]
Mazzucato, A., Papa, R., Bitocchi, E., Mosconi, P., Nanni, L., Negri, V., Picarella, M.E., Siligato, F., Soressi, G.P., Tiranti, B. and Veronesi, F. (2008) Genetic Diversity, Structure and Marker-Trait Associations in a Collection of Italian Tomato (Solanum lycopersicum L.) Landraces. Theoretical and Applied Genetics, 116, 657-669.
https://doi.org/10.1007/s00122-007-0699-6
[28]
Weigel, D. and Glazebrook, J. (2002) Arabidopsis: A Laboratory Manual Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
[29]
Golicz, A.A., Bayer, P.E. and Edwards, D. (2015) Skim-Based Genotyping by Sequencing. Methods in Molecular Biology, 1245, 257-270.
https://doi.org/10.1007/978-1-4939-1966-6_19
[30]
Langmead, B. and Salzberg, S.L. (2012) Fast Gapped-Read Alignment with Bowtie 2. Nature Methods, 9, 357-359. https://doi.org/10.1038/nmeth.1923
[31]
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Martha, G., Abecasis, G. and Durbin, R. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
https://doi.org/10.1093/bioinformatics/btp352
[32]
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. and DePristo, M.A. (2010) The Genome Analysis Toolkit: A MapReduce Framework for Analyzing Next-Generation DNA Sequencing Data. Genome Research, 20, 1297-1303.
https://doi.org/10.1101/gr.107524.110
[33]
Browning, S.R. and Browning, B.L. (2007) Rapid and Accurate Haplotype Phasing and Missing-Data Inference for Whole-Genome Association Studies by Use of Localized Haplotype Clustering. American Journal of Human Genetics, 81, 1084-1097.
https://doi.org/10.1086/521987
[34]
Pritchard, J.K., Stephens, M. and Donnelly, P. (2000) Inference of Population Structure Using Multilocus Genotype Data. Genetics, 155, 945-959.
[35]
Evanno, G., Regnaut, S. and Goudet, J. (2005) Detecting the Number of Clusters of Individuals Using the Software Structure: A Simulation Study. Molecular Ecology, 14, 2611-2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
[36]
Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y. and Buckler, E.S. (2007) TASSEL: Software for Association Mapping of Complex Traits in Diverse Samples. Bioinformatics, 23, 2633-2635.
https://doi.org/10.1093/bioinformatics/btm308
[37]
Letunic, I. and Bork, P. (2019) Interactive Tree of Life (iTOL) v4: Recent Updates and New Developments. Nucleic Acids Research, 47, W256-W259.
https://doi.org/10.1093/nar/gkz239
[38]
Causse, M., Desplat, N., Pascual, L., Le Paslier, M.C., Sauvage, C., Bauchet, G., Berard, A., Bounon, R., Tchoumakov, M., Brunel, D. and Bouchet, J.P. (2013) Whole Genome Resequencing in Tomato Reveals Variation Associated with Introgression and Breeding Events. BMC Genomics, 14, 791.
https://doi.org/10.1186/1471-2164-14-791
[39]
Blanca, J., Montero-Pau, J., Sauvage, C., Bauchet, G., Illa, E., Diez, M.J., Francis, D., Causse, M., van der Knaap, E. and Canizares, J. (2015) Genomic Variation in Tomato, from Wild Ancestors to Contemporary Breeding Accessions. BMC Genomics, 16, 257. https://doi.org/10.1186/s12864-015-1444-1
Fray, R.G. and Grierson, D. (1993) Identification and Genetic Analysis of Normal and Mutant Phytoene Synthase Genes of Tomato by Sequencing, Complementation and Co-Suppression. Plant Molecular Biology, 22, 589-602.
https://doi.org/10.1007/BF00047400
[42]
Rodriguez, G.R., Munos, S. anderson, C., Sim, S.C., Michel, A., Causse, M., Gardener, B.B., Francis, D. and van der Knaap, E. (2011) Distribution of SUN, OVATE, LC, and FAS in the Tomato Germplasm and the Relationship to Fruit Shape Diversity. Plant Physiology, 156, 275-285. https://doi.org/10.1104/pp.110.167577
[43]
Ronen, G., Carmel-Goren, L., Zamir, D. and Hirschberg, J. (2000) An Alternative Pathway to Beta-Carotene Formation in Plant Chromoplasts Discovered by Map-Based Cloning of Beta and Old-Gold Color Mutations in Tomato. Proceedings of the National Academy of Sciences, 97, 11102-11107.
https://doi.org/10.1073/pnas.190177497
[44]
Smith, P.G. (1944) Embryo Culture of a Tomato Species Hybrid. Proceedings of the American Society for Horticultural Science, 44, 413-416.
[45]
Stevens, M.R., Lamb, E.M. and Rhoads, D.D. (1995) Mapping the Sw-5 Locus for Tomato Spotted Wilt Virus-Resistance in Tomatoes Using RAPD and RFLP Analyses. Theoretical and Applied Genetics, 90, 451-456.
https://doi.org/10.1007/BF00221989
[46]
Stevens, M.R., Scott, S.J. and Gergerich, R.C.J.E. (1994) Evaluation of Seven Lycopersicon Species for Resistance to Tomato Spotted Wilt Virus (TSWV). Euphytica, 80, 79-84. https://doi.org/10.1007/BF00039301
[47]
Kalloo and Banerjee, M.K. (1990) Transfer of Tomato Leaf Curl Virus-Resistance from Lycopersicon hirsutum to L. esculentum. Plant Breeding, 105, 156-159.
https://doi.org/10.1111/j.1439-0523.1990.tb00469.x
[48]
Hanson, P.M., Bernacchi, D., Green, S., Tanksley, S.D., Muniyappa, V., Padmaja, S., Chen, H.M., Kuo, G., Fang, D. and Chen, J.T. (2000) Mapping a Wild Tomato Introgression Associated with Tomato Yellow Leaf Curl Virus Resistance in a Cultivated Tomato Line. Journal of the American Society for Horticultural Science, 125, 15-20. https://doi.org/10.21273/JASHS.125.1.15
[49]
Ji, Y., Schuster, D.J. and Scott, J.W. (2007) Ty-3, a Begomovirus Resistance Locus near the Tomato Yellow Leaf Curl Virus Resistance Locus Ty-1 on Chromosome 6 of Tomato. Molecular Breeding, 20, 271-284.
https://doi.org/10.1007/s11032-007-9089-7
[50]
Ori, N., Eshed, Y., Paran, I., Presting, G., Aviv, D., Tanksley, S., Zamir, D. and Fluhr, R. (1997) The I2C Family from the Wilt Disease Resistance Locus I2 Belongs to the Nucleotide Binding, Leucine-Rich Repeat Superfamily of Plant Resistance Genes. Plant Cell, 9, 521-532. https://doi.org/10.1105/tpc.9.4.521
[51]
Bournival, B.L., Scott, J.W. and Vallejos, C.E. (1989) An Isozyme Marker for Resistance to Race-3 of Fusarium oxysporum sp lycopersici in Tomato. Theoretical and Applied Genetics, 78, 489-494. https://doi.org/10.1007/BF00290832
[52]
Scott, J.W. and Jones, J.P. (1989) Monongenic Resistance in Tomato to Fusarium oxysporum F. sp. lycopersici Race-3. Euphytica, 40, 49-53.
