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Seeing the unseen: A trifoliate (MYB117) mutant allele fortifies folate and carotenoids in tomato fruits

Micronutrient deficiency also termed hidden hunger affects a large segment of the human population, particularly in developing and underdeveloped nations. Tomato the second most consumed vegetable crop in the world after potato can serve as a sustainable source to alleviate micronutrient deficiency. In tomato, the mutations in the R2R3-MYB117 transcription factor elicit trifoliate leaves and initiate axillary meristems; however, its effect on fruit metabolome remains unexplored. The fruits of a new trifoliate (tf) allele (tf-5) were firmer, had higher °Brix, folate, and carotenoids. The transcriptome, proteome, and metabolome profiling of tf-5 reflected a broad-spectrum change in homeostasis. The tf-5 allele enhanced the fruit firmness by suppressing cell wall softening-related proteins. The tf-5 fruit displayed a substantial increase in aminome, particularly γ-aminobutyric acid, with a parallel reduction in aminoacyl t-RNA synthases. The increased lipoxygenases proteins and transcripts seemingly elevated jasmonic acid. In addition, increased abscisic acid hydrolases transcripts coupled with reduced precursor supply lowered abscisic acid. The upregulation of carotenoids was mediated by modulation of methylerythreitol and plastoquinone pathways along with an increase in carotenoids isomerization proteins. The upregulation of folate in tf-5 was connoted by the increase in precursor p-aminobenzoic acid and transcripts of several folate biosynthesis pathway genes. The reduction in pterin-6-carboxylate and γ-glutamyl hydrolase activity indicated that the diminished folate degradation also enriched folate levels. Our study delineates that introgression of the tf-5 can be used for the γ-aminobutyric acid, carotenoids, and folate fortification of tomato. One-sentence summary A tomato trifoliate allele encoding a truncated MYB117 transcription factor alters cellular homeostasis and fortifies γ-aminobutyric acid, folate, and carotenoids in tomato fruits.