Root-sourced 1-aminocyclopropane-1-carboxylic acid modulates development and adaptive responses to salinity in tomato

Abstract

To investigate whether root-sourced ethylene-precursor 1-aminocyclopropane-1-carboxylic acid (ACC) modulates long-term salinity responses in tomato, a commercial variety (Solanum lycopersicum L. Mill) was grafted onto three rootstocks differing in ACC/ethylene production: an ethylene-overproducing mutant (epinastic, epi), a root-specific ACC deaminase overexpressing transgenic line with reduced ACC availability for ethylene synthesis (ACCD) and the wild-type cv. Micro-Tom (WT). ACCD grafts exhibited low-ACC concentrations, a branched root system and enhanced plant growth and yield stability under salinity, compared to epi and WT grafts, through modulating nutritional, metabolic, hormonal and transcriptional networks in the scion. Low root-sourced ACC was linked to down- and upregulation of ABA biosynthesis (NCED3) and catabolism (CYP707A1/3), leading to reduced leaf ABA but induced signalling; activation of GA biosynthesis (GA20ox, GA3ox) and CK homeostasis (ZOG, AHPT1L, ARR-Bs, CRF2/4); induced steroid metabolism; improved leaf P (SPX3, PAP17, PEPC1), Ca and S nutrition, and limited Na⁺ accumulation, leading to stable carbon metabolism, source–sink relations and yield under salt stress. High root-sourced ACC in epi grafts mainly penalised reproductive growth but induced protective flavonoids and source activity in salinised leaves. These findings highlight the role of root-derived ACC in modulating local and systemic responses to stress and its potential for improving crop yield stability under salinity.