Genome-wide variants and optimal allelic combinations for citric acid in tomato.

ABSTRACT

Citric acid (CA) plays a crucial role as a fruit flavor enhancer and serves as a mediator in multiple metabolic pathways in tomato fruit development. Understanding factors influencing CA metabolism is essential for enhancing fruit flavor and CA-mediated biological processes. The accumulation of CA, however, is influenced by a complex interplay of genetic and environmental factors, leading to challenges in accurately predicting and regulating its levels. In this study, we conducted a genome-wide association study (GWAS) on CA, employing six landmark models based on genome-wide variations including structural variants, insertions and deletions, and single nucleotide polymorphisms. The identification of 11 high-confidence candidate genes was further facilitated by leveraging linkage disequilibrium and causal variants associated with CA. The transcriptome data from candidate genes were examined, revealing higher correlations between the expression of certain candidate genes and changes in CA metabolism. Three CA-associated genes exerted a positive regulatory effect on CA accumulation, while the remaining genes exhibited negative impacts based on gene cluster and correlation analyses. The CA content of tomatoes is primarily influenced by improvement sweeps with minimal influence from domestication sweeps in the long-term breeding history, as evidenced by population differentiation and variants distribution. The presence of various causal variants within candidate genes is implicated in the heterogeneity of CA content observed among the tomato accessions. This observation suggests a potential correlation between the number of alternative alleles and CA content. This study offers significant function-based markers that can be utilized in marker-assisted breeding, thereby enhancing their value and applicability.