Gibberellins regulate root growth by antagonizing the jasmonate pathway in tomato plants in response to potassium deficiency

Abstract

Hormones are essential for regulating plant growth and developmental processes. Cross-talk among different hormones fine-tunes the responses to various stress. The mechanism of phytohormone-mediated root growth and development in response to potassium (K) deficiency in tomato plants remains unclear. In this study, we compared the phenotype, transcriptome and phytohormone levels between a low K+ (LK)-tolerant tomato cultivar, JZ34, and an LK-sensitive cultivar, JZ18, to understand the underlying molecular mechanism of LK-tolerance in tomato plants. Under LK stress conditions (0.5 mM K+), the root morphology traits and growth were reduced in JZ18 than those under control conditions (4 mM K+). In contrast, the changes in these traits in JZ34 were nonsignificant. The differential gene expression analysis between JZ18 plants under LK conditions on day 0 vs. day 1 (JZ18-0 vs. 18-1), JZ18-1 vs. 18-3, JZ34 plants under LK conditions on day 0 vs. day 1 (JZ34-0 vs. JZ34-1), and JZ34-1 vs. JZ34-3 identified 814, 776, 1648, and 1029 differentially expressed genes (DEGs), respectively. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway analyses demonstrated that DEGs under LK conditions were closely associated with the pathways involved in phytohormone biosynthesis and catabolism, plant hormone signal transduction, and cell wall components, which contributed to the maintenance of root growth under LK stress. Quantitative analysis of hormones using liquid chromatography-tandem mass spectrometry indicated that the over-accumulation of gibberellic acid (GA) 3 and low levels of jasmonic acid (JA) in roots accounted for root growth in JZ34. Supplementation with GA or GA synthesis inhibitor (paclobutrazol; PP333), and JA or JA biosynthesis inhibitor (diethyldithiocarbamate; DIECA) confirmed that GA3 and DIECA alleviated LK‐induced plant growth inhibition in JZ18. In contrast, JA and PP333 inhibited root growth under LK conditions. We also showed that GA antagonizes the JA responses by strongly inhibiting the transcript accumulation of MYC2, the key transcriptional activator of JA signaling. Our results reveal that GAs suppress cellular competence in response to JA in K+ deficiency stress. We show that the roots of tomato plants respond differently to LK stress, potentially due to the phytohormone-mediated pathways and mechanisms.