Exploring the Genomic Landscape: A Comprehensive Analysis of the Genetic Diversity and Population Structure of Thai Tomato Germplasm through Whole-Genome Sequencing (WGS)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials
2.2. DNA Extraction
2.3. Sequencing and SNP Discovery
2.4. Estimation of Population Parameters and Genetic Differentiation Analysis
3. Results
3.1. DNA Extraction, Sequencing and SNP Discovery
3.2. Linkage Disequilibrium (LD) Decay
3.3. Genetic Diversity and Population Structure
3.4. Principal Component Analysis (PCA)
3.5. Analysis of Population Differentiation and Analysis of Molecular Variance (AMOVA)
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Frusciante, L.; Barone, A.; Carputo, D.; Ercolano, M.R.; della Rocca, F.; Esposito, S. Evaluation and Use of Plant Biodiversity for Food and Pharmaceuticals. Fitoterapia 2000, 71, S66–S72. [Google Scholar] [CrossRef] [PubMed]
- Sim, S.-C.; Robbins, M.D.; Deynze, A.V.; Michel, A.P.; Francis, D.M. Population Structure and Genetic Differentiation Associated with Breeding History and Selection in Tomato (Solanum lycopersicum L.). Heredity 2011, 106, 927–935. [Google Scholar] [CrossRef] [PubMed]
- Bauchet, G.; Causse, M. Genetic Diversity in Tomato (Solanum lycopersicum) and Its Wild Relatives. In Genetic Diversity in Plants; Mahmut, C., Ed.; InTech: Rijeka, Croatia, 2012; ISBN 978-953-51-0185-7. [Google Scholar]
- Carbonell, P.; Alonso, A.; Grau, A.; Salinas, J.F.; García-Martínez, S.; Ruiz, J.J. Twenty Years of Tomato Breeding at EPSO-UMH: Transfer Resistance from Wild Types to Local Landraces—From the First Molecular Markers to Genotyping by Sequencing (GBS). Diversity 2018, 10, 12. [Google Scholar] [CrossRef]
- Kandel, D.R.; Bedre, R.H.; Mandadi, K.K.; Crosby, K.; Avila, C.A. Genetic Diversity and Population Structure of Tomato (Solanum lycopersicum) Germplasm Developed by Texas A&M Breeding Programs. Am. J. Plant Sci. 2019, 10, 1154–1180. [Google Scholar]
- Brbaklić, L.; Trkulja, D.; Mikić, S.; Mirosavljević, M.; Momčilović, V.; Dudić, B.; Procházková, L.; Aćin, V. Genetic Diversity and Population Structure of Serbian Barley (Hordeum vulgare L.) Collection during a 40-Year Long Breeding Period. Agronomy 2021, 11, 118. [Google Scholar] [CrossRef]
- Pandey, J.; Scheuring, D.C.; Koym, J.W.; Coombs, J.; Novy, R.G.; Thompson, A.L.; Holm, D.G.; Douches, D.S.; Miller, J.C.; Vales, M.I. Genetic Diversity and Population Structure of Advanced Clones Selected over Forty Years by a Potato Breeding Program in the USA. Sci. Rep. 2021, 11, 8344. [Google Scholar] [CrossRef] [PubMed]
- Swarup, S.; Cargill, E.J.; Crosby, K.; Flagel, L.; Kniskern, J.; Glenn, K.C. Genetic Diversity Is Indispensable for Plant Breeding to Improve Crops. Crop Sci. 2021, 61, 839–852. [Google Scholar] [CrossRef]
- Tiwari, J.K.; Yerasu, S.R.; Rai, N.; Singh, D.P.; Singh, A.K.; Karkute, S.G.; Singh, P.M.; Behera, T.K. Progress in Marker-Assisted Selection to Genomics-Assisted Breeding in Tomato. Crit. Rev. Plant Sci. 2022, 41, 321–350. [Google Scholar] [CrossRef]
- Rothan, C.; Diouf, I.; Causse, M. Trait Discovery and Editing in Tomato. Plant J. 2019, 97, 73–90. [Google Scholar] [CrossRef]
- Cappetta, E.; Andolfo, G.; Di Matteo, A.; Ercolano, M.R. Empowering Crop Resilience to Environmental Multiple Stress through the Modulation of Key Response Components. J. Plant Physiol. 2020, 246–247, 153134. [Google Scholar] [CrossRef]
- Ayenan, M.A.T.; Danquah, A.; Hanson, P.; Asante, I.K.; Danquah, E.Y. Identification of New Sources of Heat Tolerance in Cultivated and Wild Tomatoes. Euphytica 2021, 217, 33. [Google Scholar] [CrossRef]
- The 100 Tomato Genome Sequencing Consortium; Aflitos, S.; Schijlen, E.; de Jong, H.; de Ridder, D.; Smit, S.; Finkers, R.; Wang, J.; Zhang, G.; Li, N.; et al. Exploring Genetic Variation in the Tomato (Solanum Section Lycopersicon) Clade by Whole-Genome Sequencing. Plant J. 2014, 80, 136–148. [Google Scholar] [CrossRef] [PubMed]
- Al Shaye, N.; Migdadi, H.; Charbaji, A.; Alsayegh, S.; Daoud, S.; AL-Anazi, W.; Alghamdi, S. Genetic Variation among Saudi Tomato (Solanum lycopersicum L.) Landraces Studied Using SDS-PAGE and SRAP Markers. Saudi J. Biol. Sci. 2018, 25, 1007–1015. [Google Scholar] [CrossRef]
- Kiani, G.; Siahchehreh, M. Genetic Diversity in Tomato Varieties Assessed by ISSR Markers. Int. J. Veg. Sci. 2018, 24, 353–360. [Google Scholar] [CrossRef]
- Gonias, E.D.; Ganopoulos, I.; Mellidou, I.; Bibi, A.C.; Kalivas, A.; Mylona, P.V.; Osanthanunkul, M.; Tsaftaris, A.; Madesis, P.; Doulis, A.G. Exploring Genetic Diversity of Tomato (Solanum lycopersicum L.) Germplasm of Genebank Collection Employing SSR and SCAR Markers. Genet. Resour. Crop Evol. 2019, 66, 1295–1309. [Google Scholar] [CrossRef]
- Jin, L.; Zhao, L.; Wang, Y.; Zhou, R.; Song, L.; Xu, L.; Cui, X.; Li, R.; Yu, W.; Zhao, T. Genetic Diversity of 324 Cultivated Tomato Germplasm Resources Using Agronomic Traits and InDel Markers. Euphytica 2019, 215, 69. [Google Scholar] [CrossRef]
- Esposito, S.; Cardi, T.; Campanelli, G.; Sestili, S.; Díez, M.J.; Soler, S.; Prohens, J.; Tripodi, P. ddRAD Sequencing-Based Genotyping for Population Structure Analysis in Cultivated Tomato Provides New Insights into the Genomic Diversity of Mediterranean ‘Da Serbo’ Type Long Shelf-Life Germplasm. Hortic. Res. 2020, 7, 134. [Google Scholar] [CrossRef] [PubMed]
- Alzahib, R.H.; Migdadi, H.M.; Ghamdi, A.A.A.; Alwahibi, M.S.; Afzal, M.; Elharty, E.H.; Alghamdi, S.S. Exploring Genetic Variability among and within Hail Tomato Landraces Based on Sequence-Related Amplified Polymorphism Markers. Diversity 2021, 13, 135. [Google Scholar] [CrossRef]
- Kim, M.; Jung, J.-K.; Shim, E.-J.; Chung, S.-M.; Park, Y.; Lee, G.P.; Sim, S.-C. Genome-Wide SNP Discovery and Core Marker Sets for DNA Barcoding and Variety Identification in Commercial Tomato Cultivars. Sci. Hortic. 2021, 276, 109734. [Google Scholar] [CrossRef]
- Villanueva-Gutierrez, E.E.; Johansson, E.; Prieto-Linde, M.L.; Centellas Quezada, A.; Olsson, M.E.; Geleta, M. Simple Sequence Repeat Markers Reveal Genetic Diversity and Population Structure of Bolivian Wild and Cultivated Tomatoes (Solanum lycopersicum L.). Genes 2022, 13, 1505. [Google Scholar] [CrossRef]
- Pathaichindachote, W.; Panyawut, N.; Sikaewtung, K.; Patarapuwadol, S.; Muangprom, A. Genetic Diversity and Allelic Frequency of Selected Thai and Exotic Rice Germplasm Using SSR Markers. Rice Sci. 2019, 26, 393–403. [Google Scholar] [CrossRef]
- Vejchasarn, P.; Shearman, J.R.; Chaiprom, U.; Phansenee, Y.; Suthanthangjai, A.; Jairin, J.; Chamarerk, V.; Tulyananda, T.; Amornbunchornvej, C. Population Structure of Nation-Wide Rice in Thailand. Rice 2021, 14, 88. [Google Scholar] [CrossRef] [PubMed]
- Aesomnuk, W.; Ruengphayak, S.; Ruanjaichon, V.; Sreewongchai, T.; Malumpong, C.; Vanavichit, A.; Toojinda, T.; Wanchana, S.; Arikit, S. Estimation of the Genetic Diversity and Population Structure of Thailand’s Rice Landraces Using SNP Markers. Agronomy 2021, 11, 995. [Google Scholar] [CrossRef]
- Li, H.; Durbin, R. Fast and Accurate Short Read Alignment with Burrows-Wheeler Transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [PubMed]
- Danecek, P.; Bonfield, J.K.; Liddle, J.; Marshall, J.; Ohan, V.; Pollard, M.O.; Whitwham, A.; Keane, T.; McCarthy, S.A.; Davies, R.M.; et al. Twelve Years of SAMtools and BCFtools. GigaScience 2021, 10, giab008. [Google Scholar] [CrossRef] [PubMed]
- Van der Auwera, G.A.; O’Connor, B.D. Genomics in the Cloud: Using Docker, GATK, and WDL in Terra; O’Reilly Media: Sebastopol, CA, USA, 2020; ISBN 1-4919-7516-4. [Google Scholar]
- Danecek, P.; Auton, A.; Abecasis, G.; Albers, C.A.; Banks, E.; DePristo, M.A.; Handsaker, R.E.; Lunter, G.; Marth, G.T.; Sherry, S.T.; et al. The Variant Call Format and VCFtools. Bioinformatics 2011, 27, 2156–2158. [Google Scholar] [CrossRef] [PubMed]
- Yin, L.; Zhang, H.; Tang, Z.; Xu, J.; Yin, D.; Zhang, Z.; Yuan, X.; Zhu, M.; Zhao, S.; Li, X.; et al. rMVP: A Memory-Efficient, Visualization-Enhanced, and Parallel-Accelerated Tool for Genome-Wide Association Study. Genom. Proteom. Bioinform. 2021, 19, 619–628. [Google Scholar] [CrossRef]
- Zhang, C.; Dong, S.-S.; Xu, J.-Y.; He, W.-M.; Yang, T.-L. PopLDdecay: A Fast and Effective Tool for Linkage Disequilibrium Decay Analysis Based on Variant Call Format Files. Bioinformatics 2019, 35, 1786–1788. [Google Scholar] [CrossRef] [PubMed]
- Cook, D.E.; Andersen, E.C. VCF-Kit: Assorted Utilities for the Variant Call Format. Bioinformatics 2017, 33, 1581–1582. [Google Scholar] [CrossRef]
- Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef]
- Raj, A.; Stephens, M.; Pritchard, J.K. fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets. Genetics 2014, 197, 573–589. [Google Scholar] [CrossRef] [PubMed]
- Chang, C.C.; Chow, C.C.; Tellier, L.C.; Vattikuti, S.; Purcell, S.M.; Lee, J.J. Second-Generation PLINK: Rising to the Challenge of Larger and Richer Datasets. GigaScience 2015, 4, 7. [Google Scholar] [CrossRef] [PubMed]
- Goudet, J. Hierfstat, a Package for r to Compute and Test Hierarchical F-Statistics. Mol. Ecol. Notes 2005, 5, 184–186. [Google Scholar] [CrossRef]
- Kamvar, Z.N.; Tabima, J.F.; Grünwald, N.J. Poppr: An R Package for Genetic Analysis of Populations with Clonal, Partially Clonal, and/or Sexual Reproduction. PeerJ 2014, 2, e281. [Google Scholar] [CrossRef] [PubMed]
- Labate, J.A. DNA Variation in a Diversity Panel of Tomato Genetic Resources. J. Am. Soc. Hortic. Sci. 2021, 146, 339–345. [Google Scholar] [CrossRef]
- Caramante, M.; Rouphael, Y.; Corrado, G. Genetic Diversity among and within Tomato (Solanum lycopersicum L.) Landraces Grown in Southern Italy. Genet. Resour. Crop Evol. 2023, 71, 157–166. [Google Scholar] [CrossRef]
- Sim, S.-C.; Durstewitz, G.; Plieske, J.; Wieseke, R.; Ganal, M.W.; Van Deynze, A.; Hamilton, J.P.; Buell, C.R.; Causse, M.; Wijeratne, S.; et al. Development of a Large SNP Genotyping Array and Generation of High-Density Genetic Maps in Tomato. PLoS ONE 2012, 7, e40563. [Google Scholar] [CrossRef]
- Lin, Y.-P.; Liu, C.-Y.; Chen, K.-Y. Assessment of Genetic Differentiation and Linkage Disequilibrium in Solanum pimpinellifolium Using Genome-Wide High-Density SNP Markers. G3 GenesGenomesGenetics 2019, 9, 1497–1505. [Google Scholar] [CrossRef]
- Bauchet, G.; Grenier, S.; Samson, N.; Bonnet, J.; Grivet, L.; Causse, M. Use of Modern Tomato Breeding Germplasm for Deciphering the Genetic Control of Agronomical Traits by Genome Wide Association Study. Theor. Appl. Genet. 2017, 130, 875–889. [Google Scholar] [CrossRef]
- van Berloo, R.; Zhu, A.; Ursem, R.; Verbakel, H.; Gort, G.; van Eeuwijk, F.A. Diversity and Linkage Disequilibrium Analysis within a Selected Set of Cultivated Tomatoes. Theor. Appl. Genet. 2008, 117, 89–101. [Google Scholar] [CrossRef]
- Robbins, M.D.; Sim, S.-C.; Yang, W.; Van Deynze, A.; van der Knaap, E.; Joobeur, T.; Francis, D.M. Mapping and Linkage Disequilibrium Analysis with a Genome-Wide Collection of SNPs That Detect Polymorphism in Cultivated Tomato. J. Exp. Bot. 2011, 62, 1831–1845. [Google Scholar] [CrossRef] [PubMed]
- Sim, S.-C.; Van Deynze, A.; Stoffel, K.; Douches, D.S.; Zarka, D.; Ganal, M.W.; Chetelat, R.T.; Hutton, S.F.; Scott, J.W.; Gardner, R.G.; et al. High-Density SNP Genotyping of Tomato (Solanum lycopersicum L.) Reveals Patterns of Genetic Variation Due to Breeding. PLoS ONE 2012, 7, e45520. [Google Scholar] [CrossRef] [PubMed]
- Brake, M.; Al-Qadumii, L.; Hamasha, H.; Migdadi, H.; Awad, A.; Haddad, N.; Sadder, M.T. Development of SSR Markers Linked to Stress Responsive Genes along Tomato Chromosome 3 (Solanum lycopersicum L.). BioTech 2022, 11, 34. [Google Scholar] [CrossRef]
- Chen, L.; Li, W.; Li, Y.; Feng, X.; Du, K.; Wang, G.; Zhao, L. Identified Trans-Splicing of YELLOW-FRUITED TOMATO 2 Encoding the PHYTOENE SYNTHASE 1 Protein Alters Fruit Color by Map-Based Cloning, Functional Complementation and RACE. Plant Mol. Biol. 2019, 100, 647–658. [Google Scholar] [CrossRef] [PubMed]
- Mata-Nicolás, E.; Montero-Pau, J.; Gimeno-Paez, E.; Garcia-Carpintero, V.; Ziarsolo, P.; Menda, N.; Mueller, L.A.; Blanca, J.; Cañizares, J.; van der Knaap, E.; et al. Exploiting the Diversity of Tomato: The Development of a Phenotypically and Genetically Detailed Germplasm Collection. Hortic. Res. 2020, 7, 66. [Google Scholar] [CrossRef] [PubMed]
- Çolak, N.G.; Eken, N.T.; Ülger, M.; Frary, A.; Doğanlar, S. Mapping of Quantitative Trait Loci for the Nutritional Value of Fresh Market Tomato. Funct. Integr. Genom. 2023, 23, 121. [Google Scholar] [CrossRef] [PubMed]
- de Souza, L.M.; Paterniani, M.E.A.; Melo, P.C.T.; de Melo, A.M. Diallel Cross among Fresh Market Tomato Inbreeding Lines. Hortic. Bras. 2012, 30, 246–251. [Google Scholar] [CrossRef]
- Bergougnoux, V. The History of Tomato: From Domestication to Biopharming. Biotechnol. Adv. 2014, 32, 170–189. [Google Scholar] [CrossRef]
- Sun, L.; Chen, J.; Xiao, K.; Yang, W. Origin of the Domesticated Horticultural Species and Molecular Bases of Fruit Shape and Size Changes during the Domestication, Taking Tomato as an Example. Hortic. Plant J. 2017, 3, 125–132. [Google Scholar] [CrossRef]
- Lin, T.; Zhu, G.; Zhang, J.; Xu, X.; Yu, Q.; Zheng, Z.; Zhang, Z.; Lun, Y.; Li, S.; Wang, X.; et al. Genomic Analyses Provide Insights into the History of Tomato Breeding. Nat. Genet. 2014, 46, 1220–1226. [Google Scholar] [CrossRef]
- Zhu, G.; Wang, S.; Huang, Z.; Zhang, S.; Liao, Q.; Zhang, C.; Lin, T.; Qin, M.; Peng, M.; Yang, C.; et al. Rewiring of the Fruit Metabolome in Tomato Breeding. Cell 2018, 172, 249–261.e12. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Hu, S.; Gardner, C.; Lübberstedt, T. Emerging Avenues for Utilization of Exotic Germplasm. Trends Plant Sci. 2017, 22, 624–637. [Google Scholar] [CrossRef] [PubMed]
- Schouten, H.J.; Tikunov, Y.; Verkerke, W.; Finkers, R.; Bovy, A.; Bai, Y.; Visser, R.G.F. Breeding Has Increased the Diversity of Cultivated Tomato in The Netherlands. Front. Plant Sci. 2019, 10, 1606. [Google Scholar] [CrossRef] [PubMed]
- Sumalan, R.M.; Ciulca, S.I.; Poiana, M.A.; Moigradean, D.; Radulov, I.; Negrea, M.; Crisan, M.E.; Copolovici, L.; Sumalan, R.L. The Antioxidant Profile Evaluation of Some Tomato Landraces with Soil Salinity Tolerance Correlated with High Nutraceuticaland Functional Value. Agronomy 2020, 10, 500. [Google Scholar] [CrossRef]
- Rouphael, Y.; Corrado, G.; Colla, G.; De Pascale, S.; Dell’Aversana, E.; D’Amelia, L.I.; Fusco, G.M.; Carillo, P. Biostimulation as a Means for Optimizing Fruit Phytochemical Content and Functional Quality of Tomato Landraces of the San Marzano Area. Foods 2021, 10, 926. [Google Scholar] [CrossRef]
- Tiwari, J.K.; Singh, A.K.; Behera, T.K. CRISPR/Cas Genome Editing in Tomato Improvement: Advances and Applications. Front. Plant Sci. 2023, 14, 1121209. [Google Scholar] [CrossRef]
Admixture Group | Cherry | Table | TH | INT |
---|---|---|---|---|
Q1 | 1 | 10 | 6 | 5 |
Q2 | 0 | 10 | 0 | 10 |
Q3 | 5 | 0 | 1 | 4 |
Q4 | 14 | 28 | 2 | 40 |
Q5 | 2 | 8 | 1 | 9 |
Q6 | 1 | 7 | 2 | 6 |
Q7 | 16 | 0 | 15 | 1 |
Q8 | 13 | 0 | 11 | 2 |
Q9 | 6 | 0 | 2 | 4 |
Q10 | 4 | 11 | 15 | 0 |
Q11 | 2 | 7 | 3 | 6 |
Q12 | 3 | 0 | 0 | 3 |
admix | 78 | 57 | 50 | 85 |
Source of Variation | df | Sum Sq. | Mean Sq. | Sigma | Percentage of Total Variance |
---|---|---|---|---|---|
Between populations | 1 | 3683.59 | 3683.590 | 13.53806 | 0.7167299 |
Within populations | 281 | 526,966.71 | 1875.326 | 1875.32638 | 99.2832701 |
Total | 282 | 530,650.30 | 1881.739 | 1888.86444 | 100.0000000 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yongsuwan, A.; Poncheewin, W.; Sastawittaya, W.; Somkul, A.; Thunnom, B.; Aesomnuk, W.; Bhunchoth, A.; Phironrit, N.; Phuangrat, B.; Koohapitakthum, R.; et al. Exploring the Genomic Landscape: A Comprehensive Analysis of the Genetic Diversity and Population Structure of Thai Tomato Germplasm through Whole-Genome Sequencing (WGS). Horticulturae 2024, 10, 602. https://doi.org/10.3390/horticulturae10060602
Yongsuwan A, Poncheewin W, Sastawittaya W, Somkul A, Thunnom B, Aesomnuk W, Bhunchoth A, Phironrit N, Phuangrat B, Koohapitakthum R, et al. Exploring the Genomic Landscape: A Comprehensive Analysis of the Genetic Diversity and Population Structure of Thai Tomato Germplasm through Whole-Genome Sequencing (WGS). Horticulturae. 2024; 10(6):602. https://doi.org/10.3390/horticulturae10060602
Chicago/Turabian StyleYongsuwan, Arweewut, Wasin Poncheewin, Wittaya Sastawittaya, Akarachai Somkul, Burin Thunnom, Wanchana Aesomnuk, Anjana Bhunchoth, Namthip Phironrit, Bencharong Phuangrat, Ratree Koohapitakthum, and et al. 2024. "Exploring the Genomic Landscape: A Comprehensive Analysis of the Genetic Diversity and Population Structure of Thai Tomato Germplasm through Whole-Genome Sequencing (WGS)" Horticulturae 10, no. 6: 602. https://doi.org/10.3390/horticulturae10060602
APA StyleYongsuwan, A., Poncheewin, W., Sastawittaya, W., Somkul, A., Thunnom, B., Aesomnuk, W., Bhunchoth, A., Phironrit, N., Phuangrat, B., Koohapitakthum, R., Deeto, R., Warin, N., Wanchana, S., Arikit, S., Chatchawankanphanich, O., Chuenwarin, P., & Ruanjaichon, V. (2024). Exploring the Genomic Landscape: A Comprehensive Analysis of the Genetic Diversity and Population Structure of Thai Tomato Germplasm through Whole-Genome Sequencing (WGS). Horticulturae, 10(6), 602. https://doi.org/10.3390/horticulturae10060602