Leaf ontogeny modulates epinasty through shifts in hormone dynamics during waterlogging in tomato

Waterlogging 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 cover a large group of growth regulators, we performed a tissue-specific and time-dependent hormonomics analysis. This revealed that multiple hormones are differentially affected throughout a 48 h waterlogging treatment, and that leaf age determines hormone homeostasis and modulates their changes during waterlogging. In addition, we distinguished early hormonal signals that contribute to fast responses to oxygen deprivation from those that potentially sustain the waterlogging response. We found that abscisic acid (ABA) levels peak in petioles within the first 12 h of the treatment, while its precursors only increase much later, suggesting that ABA transport is altered. At the same time, cytokinins (CKs) and their derivatives drastically decline during waterlogging in leaves of all ages. This drop in CKs 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 as an early signal to induce epinasty, while the balance of indole-3-acetic acid and CKs in the petiole ultimately regulates differential growth. Our work reveals phytohormone dynamics of tomato leaves during waterlogging that govern leaf epinasty. We provide evidence for the role of cytokinins and abscisic acid in regulated leaf posture control.

Automated summary

Waterlogging-induced hypoxia in the root zone leads to adaptive responses in the shoot, such as leaf epinasty. This study analyzed the dynamics of multiple hormones in tomato leaves during waterlogging, revealing that leaf age determines hormone homeostasis and modulates changes during waterlogging. Early hormonal signals, including ethylene and abscisic acid, were found to induce epinasty, while the balance of indole-3-acetic acid and cytokinins in the petiole ultimately regulates differential growth.