A novel tomato interspecific (Solanum lycopersicum var. cerasiforme and Solanum pimpinellifolium) MAGIC population facilitates trait association and candidate gene discovery in untapped exotic germplasm

Abstract

We developed a novel eight-way tomato multiparental advanced generation intercross (MAGIC) population to improve the accessibility of tomato relatives genetic resources to geneticists and breeders. The interspecific tomato MAGIC population (ToMAGIC) was obtained by intercrossing four accessions each of Solanum lycopersicum var. cerasiforme and Solanum pimpinellifolium, which are the weedy relative and the ancestor of cultivated tomato, respectively. The eight exotic ToMAGIC founders were selected based on a representation of the genetic diversity and geographical distribution of the two taxa. The resulting MAGIC population comprises 354 lines, which were genotyped using a new 12k tomato single primer enrichment technology panel and yielded 6488 high-quality single-nucleotide polymorphism (SNPs). The genotyping data revealed a high degree of homozygosity, an absence of genetic structure, and a balanced representation of the founder genomes. To evaluate the potential of the ToMAGIC population, a proof of concept was conducted by phenotyping it for fruit size, plant pigmentation, leaf morphology, and earliness. Genome-wide association studies identified strong associations for the studied traits, pinpointing both previously identified and novel candidate genes near or within the linkage disequilibrium blocks. Domesticated alleles for fruit size were recessive and were found, at low frequencies, in wild/ancestral populations. Our findings demonstrate that the newly developed ToMAGIC population is a valuable resource for genetic research in tomato, offering significant potential for identifying new genes that govern key traits in tomato. ToMAGIC lines displaying a pyramiding of traits of interest could have direct applicability for integration into breeding pipelines providing untapped variation for tomato breeding.

Acknowledgements

This work was supported by grant PID2020-118627RB-I00 funded by MICIU/AEI/10.13039/501100011033, TED2021-129296B-I00 funded by MCIN/AEI/10.13039/501100011033 and European Union Europea NextGenerationEU/PRTR, CIPROM/2021/020 funded by Conselleria d’Innovació, Universitats, Ciència i Societat Digital of the Generalitat Valenciana, the HARNESSTOM innovation action (grant agreement no. 101000716) funded by the European Commission H2020 Research and Innovation Programme, and the Horizon Europe PRO-GRACE project (grant agreement no. 10194738). Andrea Arrones is grateful to Spanish Ministerio de Ciencia, Innovación y Universidades for a predoctoral (FPU18/01742) contract. Oussama Antar is grateful to Conselleria d'Innovació, Ciència i Societat Digital of the Generalitat Valenciana for a predoctoral grant within the Santiago Grisolía program (CIGRIS/2021/113). Leandro Pereira-Dias is grateful to Universitat Politècnica de Valencia and the Spanish Ministerio de Universidades for a post-doctoral grant under the Margarita Salas funded by the European Union NextGenerationEU/PRTR. Andrea Solana is grateful to Spanish Ministerio de Ciencia e Innovación for a predoctoral grant (PRE2022-102368) funded by MCIN/AEI/10.13039/501100011033 and FSE+. Pietro Gramazio is grateful to Spanish Ministerio de Ciencia e Innovación for a post-doctoral grant (RYC2021-031999-I) funded by MCIN/AEI/10.13039/501100011033 and the European Union through NextGenerationEU/PRTR. Funding for open access: Universitat Politècnica de València.

Author contributions

S.V., P.G., M.J.D., and J.P. conceived the idea and supervised the manuscript; A.A., O.A., L.P.-D., A.S., and M.J.D. performed the field trials. G.A. and G.G. in collaboration with TECAN Genomics designed the 12k SPET panel. All authors analysed the results. A.A. and O.A. prepared a first draft of the manuscript, and the rest of the authors reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Data availability

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi.nlm.nih.gov/, PRJNA616074 (founders resequencing data), and PRJNA1103671 (ToMAGIC lines genotyping).

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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