Exploiting the diversity of tomato: the development of a phenotypically and genetically detailed germplasm collection

Mata-Nicolás et al. Horticulture Research (2020)7:66 https://doi.org/10.1038/s41438-020-0291-7 ARTICLE Horticulture Research www.nature.com/hortres Open Access Exploiting the diversity of tomato: the development of a phenotypically and genetically detailed germplasm collection 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Estefanía Mata-Nicolás1, Javier Montero-Pau 2, Esther Gimeno-Paez1, Víctor Garcia-Carpintero1, Peio Ziarsolo1, Naama Menda3, Lukas A. Mueller3, José Blanca1, Joaquín Cañizares1, Esther van der Knaap4,5 and María José Díez1 Abstract A collection of 163 accessions, including Solanum pimpinellifolium, Solanum lycopersicum var. cerasiforme and Solanum lycopersicum var. lycopersicum, was selected to represent the genetic and morphological variability of tomato at its centers of origin and domestication: Andean regions of Peru and Ecuador and Mesoamerica. The collection is enriched with S. lycopersicum var. cerasiforme from the Amazonian region that has not been analyzed previously nor used extensively. The collection has been morphologically characterized showing diversity for fruit, flower and vegetative traits. Their genomes were sequenced in the Varitome project and are publicly available (solgenomics.net/projects/ varitome). The identified SNPs have been annotated with respect to their impact and a total number of 37,974 out of 19,364,146 SNPs have been described as high impact by the SnpEeff analysis. GWAS has shown associations for different traits, demonstrating the potential of this collection for this kind of analysis. We have not only identified known QTLs and genes, but also new regions associated with traits such as fruit color, number of flowers per inflorescence or inflorescence architecture. To speed up and facilitate the use of this information, F2 populations were constructed by crossing the whole collection with three different parents. This F2 collection is useful for testing SNPs identified by GWAs, selection sweeps or any other candidate gene. All data is available on Solanaceae Genomics Network and the accession and F2 seeds are freely available at COMAV and at TGRC genebanks. All these resources together make this collection a good candidate for genetic studies. Introduction Tomato, Solanum lycopersicum var. lycopersicum L. (SLL), is one of the most consumed vegetables all over the world with a production that exceeds 180 million tonnes (FAO, 2017). Its cultivation has become highly efficient thanks to the introduction of technological advances and the development of modern varieties. These modern varieties are the result of intensive plant breeding programs since the beginning of the 20th century, and the Correspondence: Joaquín Cañizares () 1 Instituto Universitario de Conservación y Mejora de la Agrodiversidad Valenciana. COMAV. Universitat Politècnica de València, Valencia, Spain 2 Department of Biochemistry and Molecular Biology, Universitat de València, Valencia, Spain Full list of author information is available at the end of the article natural biodiversity of tomato wild species has been key in this success. The cultivated tomato and its wild relatives came from the Peruvian and Ecuadorian regions of South America. According to allozyme variation, Rick and Fobes1 proposed that SLL evolved from S. lycopersicum var. cerasiforme (Dunal) Spooner, G.J. Anderson & R.K. Jansen (SLC). Recently, Blanca et al.2,3 proposed a two-step domestication process from SLC to SLL based on molecular and morphological evidence. The first step involves the pre-domestication of SLC in the Amazonian region of Southern Ecuador and Northern Peru. Subsequently, SLC would have migrated to Mesoamerica where it would be domesticated to SLL. Razifard et al.4 proposed that many traits considered typical of cultivated tomatoes arose in © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Mata-Nicolás et al. Horticulture Research (2020)7:66 South America. However, these domestication traits were lost or diminished once these partially domesticated forms spread to Mesoamerica, where it was finally morphed into the SLL5,6. This domestication and diffusion process was accompanied by a selection of alleles related to fruit color, size and shape and also changes in plant architecture7–10. This process also included various genetic bottlenecks that progressively narrowed the genetic diversity of modern tomato, compared to its wild species3,11. The main loss of variability occurred during the migration to Mesoamerica from the Peruvian and Ecuadorian Amazon region. Most of the allelic variants present in european vintage tomato are already present in these Amazonian SLC populations3. Solanum pimpinellifolium L. (SP) is the closest wild relative to SLC and SLL. It is also a red-fruited species and native to coastal areas from Ecuador to Southern Peru. According to its distribution, this species presents varying degrees of genetic variation12–15 and morphological differences such as flower and inflorescence size, style exertion, or fruit color12. This fact and its capacity to hybridize with tomato, make this species a valuable source of desired traits in tomato breeding. For instance, SP has been used as a genetic source for quality improvement related to solid content, firmness, fruit color16,17, volatile compounds18,19, or resistance against fungi or viruses such as Tomato leaf curl virus20, Alternaria solani, Fusarium oxysporum, and Phytophthora infestans21 or Cladosporium fulvum22. SLC has a worldwide distribution in tropical regions, but it is native to the Andean region of Ecuador and North of Peru1. This species is found over a vast range of environmental conditions such as tropical or arid regions, sea level or high altitudes23, and it has also been collected at native markets24. It usually bears red and small fruits, but Rick and Holle25 described a remarkable morphological variability in fruits, plant habit, or leaf size and shape. A higher genetic variability has been described in Ecuadorian and Peruvian accessions1,2 due to the development of morphological diversity during a predomestication phase. In fact, tomatoes collected in loca (...truncated)