Mutations in the PGAM1 gene, encoding phosphoglycerate mutase-like protein 1, result in cold tolerance in the tomato plant mutant ‘cr-1′

Cold stress is a major factor limiting tomato productivity. New cold-tolerant varieties must be developed to reduce yield losses. In this study, a cold-tolerant tomato plant mutant ‘cr-1′ previously developed using ethylmethane sulfonate (EMS) was characterized at the physiological, biochemical, and omics levels. The genetic background of ‘cr-1′ (F2 generation) and its wild type (WT) ‘Moneymaker (MM)’ was analyzed, and a key gene controlling the cold tolerance was mapped to the chromosome of the tomato plant mutant ‘cr-1′ using genome-wide association studies (GWAS). Our study revealed that the ‘cr-1′ mutant exhibited mild leaf curling, low hydrogen peroxide (H₂O₂) and superoxide (O₂-) levels, and high antioxidant enzyme activities under cold stress. Combined analysis of the transcriptome and metabolome showed the accumulation of amino acids and their derivatives and stimulation of secondary metabolic pathways such as oxidative phosphorylation, zeatin biosynthesis, and biosynthesis of unsaturated fatty acids in the ‘cr-1′ mutant under cold stress. Further analysis suggested that the ‘cr-1′ mutant has a dominant genetic pattern controlled by a single gene and 5 single nucleotide polymorphism (SNP) mutations on the sixth and eighth exons of the PGAM1 (LOC101266024) gene, encoding phosphoglycerate mutase-like protein 1. These observations suggest that PGAM1 may be responsible for the mutant's cold tolerance, and the gene mutation probably improves the cold tolerance by promoting sugar accumulation. Thus, the study suggests that the ‘cr-1’ mutant is a valuable resource for breeding and developing novel cold-tolerant tomato cultivars.