Mutations in Tomato ACC Synthase2 Uncover Its Role in Development beside Fruit Ripening

ABSTRACT The role of ethylene in plant development is mostly inferred from its exogenous application. The usage of the mutants affecting ethylene biosynthesis proffers a better alternative to decipher its role. In tomato, 1-aminocyclopropane carboxylic acid synthase2 (ACS2) is a key enzyme regulating ripening-specific ethylene biosynthesis. We characterized two contrasting acs2 mutants; acs2-1 overproduces ethylene, has higher ACS activity, and increased protein levels, while acs2-2 is an ethylene under-producer, displays lower ACS activity, and protein levels than wild type. Consistent with high/low ethylene emission, the mutants show opposite phenotypes, physiological responses, and metabolomic profiles than the wild type. The acs2-1 showed early seed germination, faster leaf senescence, and accelerated fruit ripening. Conversely, acs2-2 had delayed seed germination, slower leaf senescence, and prolonged fruit ripening. The phytohormone profiles of mutants were mostly opposite in the leaves and fruits. The faster/slower senescence of acs2-1 / acs2-2 leaves correlated with the endogenous ethylene/zeatin ratio. The genetic analysis showed that the metabolite profiles of respective mutants co-segregated with the homozygous mutant progeny. Our results uncover that besides ripening, ACS2 participates in vegetative and reproductive development of tomato. The distinct influence of ethylene on phytohormone profiles indicates intertwining of ethylene action with other phytohormones in regulating plant development.