Tomato root senses horizontal/vertical mechanical impedance and correspondingly modulates root/shoot metabolome

Abstract

Plant root encounters coarse environs right after emergence from the seed. Little is known about the metabolic changes enabling the root to overcome the soil impedance. It is also not known whether roots respond differently to soil hardness when grown in the horizontal and vertical orientation. We grew tomato (Solanum lycopersicum) seedlings vertically or horizontally on agarose with increasing hardness (0.2 % → 1.2 %). We examined the morphology of roots and shoots of the seedling and also profiled phytohormones, primary metabolite levels, and transcript levels of related genes from the respective organs. Tomato seedlings grown vertically or horizontally, on agarose with increasing hardness, exhibited lateral roots proliferation, shorter hypocotyl, and primary root. In primary root tip, hardness increase elicited loss of amyloplast staining; induced reactive oxygen species, and nitric oxide accumulation. The level of indole butyric acid, zeatin, jasmonates, and salicylic acid markedly differed in root and shoot exposed to increasing hardness. Increasing hardness lowered indole acetic acid and elevated abscisic acid level, while increased ethylene emission was confined to the horizontally-impeded seedling. The trajectories of metabolomic shift distinctly differed between vertically/horizontally-impeded root/shoot. In the horizontal root, amino acids were the major affected group, while in the vertical root, sugars were the major group. Commonly affected metabolites in root and shoot, trehalose, dopamine, caffeoylquinic acid, and suberic acid, hallmarked the signature for hardness. Increasing hardness lowered Snf1-related protein kinase1a (SnRK1a) expression in root/shoot implying regulation of metabolic homeostasis by the SnRK1 signalling module. The lower E2Fa expression may lead to growth inhibition by reduced meristematic activity. Our study highlights the importance of metabolic homeostasis in facilitating root ramification in the soil. Though hardness is a common denominator, root distinguishes the horizontal/vertical orientation and correspondingly modulates metabolites level. Altogether, the data uncovers ABA, E2Fa, and SnRK1 as key regulators of hardness-induced growth inhibition of tomato seedlings.