Leaf ontogeny steers ethylene and auxin crosstalk to regulate leaf epinasty during waterlogging of tomato

Developing leaves undergo a vast array of age-related changes as they mature. These include physiological, hormonal and morphological changes that determine their adaptation plasticity towards adverse conditions. Waterlogging induces leaf epinasty in tomato, and the magnitude of leaf bending is intricately related to the age-dependent cellular and hormonal response. We now show that ethylene, the master regulator of epinasty, is differentially regulated throughout leaf development, giving rise to age-dependent epinastic responses. Young leaves have a higher basal ethylene production, but are less responsive to waterlogging-induced epinasty, as they have a higher capacity to convert the root-borne and mobilized ACC into the inactive conjugate MACC. Ethylene stimulates cell elongation relatively more at the adaxial petiole side, by activating auxin biosynthesis and locally inhibiting its transport through PIN4 and PIN9 in older and mature leaves. As a result, auxins accumulate in the petiole base of these leaves and enforce partially irreversible epinastic bending upon waterlogging. Young leaves maintain their potential to transport auxins, both locally and through the vascular tissue, leading to enhanced flexibility to dampen the epinastic response and a faster upwards repositioning during reoxygenation. This mechanism also explains the observed reduction of epinasty during and its recovery after waterlogging in the anthocyanin reduced (are) and Never ripe (Nr) mutants, both characterized by higher auxin flow. Our work has demonstrated that waterlogging activates intricate hormonal crosstalk between ethylene and auxin, controlled in an age-dependent way.