Waterlogging shifts ontogenic hormone dynamics in tomato leaves and petioles

Abstract

AbstractWaterlogging leads to hypoxic conditions in the root zone that subsequently cause systemic adaptive responses in the shoot, including leaf epinasty. Waterlogging-induced epinasty in tomato has long been ascribed to the coordinated action of ethylene and auxins. However, other hormonal signals have largely been neglected, despite evidence of their importance in leaf posture control. To adequately cover a large group of growth regulators, we performed a tissue-specific and time-dependent hormonomics analysis. This analysis revealed that multiple hormones are differentially affected throughout a 48 h waterlogging treatment, and, more importantly, that leaf development defines a framework in which this hormonal control is regulated. In addition, we could distinguish early hormonal signals that might contribute to fast responses towards oxygen deprivation from those that potentially sustain the waterlogging response. For example, abscisic acid (ABA) levels peak in petioles within the first 12 h of the treatment, while its metabolites only rise much later, suggesting ABA transport is altered. At the same time, cytokinins (CK) and their derivatives drastically decline during waterlogging in leaves of all ages. This drop in CK possibly releases the inhibition of ethylene and auxin mediated cell elongation to establish epinastic bending. Auxins themselves rise substantially in the petiole of mature leaves, but mostly after 48 h of root hypoxia. Based on our hormone profiling, we propose that ethylene and ABA might act synergistically to dynamically fine-tune the balance of IAA and CK in the petiole, ultimately leading to differential growth and epinasty during waterlogging.