Multiple-model GWAS identifies optimal allelic combinations of quantitative trait loci for malic acid in tomato

Abstract

Malic acid (MA) is an important flavor acid in fruits and acts as a mediator in a series of metabolic pathways. It is important to understand the factors affecting MA metabolism for fruit flavor improvement and to understand MA-mediated biological processes. However, the metabolic accumulation of MA is controlled by complex heredity and environmental factors, making it difficult to predict and regulate the metabolism of MA. In this study, we carried out a genome-wide association study (GWAS) on MA using eight milestone models with two-environment repeats. A series of associated SNP variations were identified from the GWAS, and 15 high-confidence annotated genes were further predicted based on linkage disequilibrium and lead SNPs. The transcriptome data of candidate genes were explored within different tomato organs as well as various fruit tissues, and suggested specific expression patterns in fruit pericarp. Based on the genetic parameters of population differentiation and SNP distribution, tomato MA content has been more influenced by domestication sweeps and less affected by improvement sweeps in the long-term history of tomato breeding. In addition, genotype × environment interaction might contribute to the difference in domestication phenotypic data under different environments. This study provides new genetic insights into how tomato changed its MA content during breeding and makes available function-based markers for breeding by marker-assisted selection.

Acknowledgements

This work was supported by grants from the National Key Research & Development Plan (2022YFD1200502; 2021YFD120 0201); the National Natural Science Foundation of China (31972426; 31991182); the Wuhan Biological Breeding Major Project (2022021302024852); the Key Project of Hubei Hongshan Laboratory (2021hszd007); the Hubei Key Research & Devel- opment Plan (2022BBA0062; 2022BBA0066); the Fundamental Research Funds for the Central Universities (2662022YLPY001) and the International Cooperation Promotion Plan of Shihezi University (GJHZ202104).

Author contributions

W.G. and Y.Z. conceived and designed the experiments. W.G. and F.Y. analyzed the data and carried on the analyses. J.T. and X.Z. performed the data collection. S.H., Yaru W., Ying W., F.Y., L.Y., L.S., F.L., P.G., F.W. and H.D. conducted the literature review and edited the manuscript. Y.Z. was responsible for funding acquisition and article revision.

Data availability

The datasets supporting the findings in this study are available in the supplementary materials.

Conflict of interest

The authors declare no competing interests.

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