An SMR cell-cycle inhibitor inducible by a carotenoid metabolite resets root development and drought tolerance in Arabidopsis

New regulatory functions in plant development and environmental stress responses have recently emerged for a number of apocarotenoids produced by enzymatic or non-enzymatic oxidation of carotenoids. {beta}-cyclocitric acid ({beta}-CCA) is one such compound derived from {beta}-carotene which triggers defense mechanisms leading to a marked enhancement of plant tolerance to drought stress. We show here that this response is associated with an inhibition of root growth affecting both root cell elongation and division. Remarkably, {beta}-CCA selectively induced cell cycle inhibitors of the SIAMESE-RELATED (SMR) family, especially SMR5, in root tip cells. Overexpression of the SMR5 gene in Arabidopsis induced molecular and physiological changes that mimicked in large part the effects of {beta}-CCA. In particular, the SMR5 overexpressors exhibited an inhibition of root development and a marked increase in drought tolerance which is not related to stomatal closure. SMR5 up-regulation induced changes in gene expression that strongly overlapped with the {beta}-CCA-induced transcriptomic changes. Both {beta}-CCA and SMR5 led to a down-regulation of many cell cycle activators (cyclins, cyclin-dependent kinases) and a concomitant up-regulation of genes related to water deprivation, cellular detoxification and biosynthesis of lipid biopolymers such as suberin and lignin. This was correlated with an accumulation of suberin lipid polyesters in the roots and a decrease in non-stomatal leaf transpiration. Taken together, our results identify the {beta}-CCA-and drought-inducible SMR5 gene as a key component of a stress signaling pathway that reorients root metabolism from growth to multiple defense mechanisms leading to drought tolerance.