Rapid formation of adventitious roots and partial ethylene sensitivity result in faster adaptation to flooding in the aerial roots (aer) mutant of tomato

•Aer mutant is characterized by fast formation of adventitious roots under flooding.•Aer mutant rapidly regains biomass accumulation after the onset of flooding.•Lower ethylene sensitivity contributes to adaptation to flooding in aer mutant.•Aer mutant proved a useful tool to study the adaptive importance of ARs.

The frequency of extreme events such as droughts and floods has increased as a consequence of climate change. Many crops have not been improved to tolerate soil anoxia and, therefore, floods cause important economic losses. During submergence, Solanum lycopersicum L. exhibits three distinct responses which are adventitious root production, epinasty and aerenchyma formation. The development of a new adventitious root system is crucial as it can replace the original roots that succumb to the hypoxic environment. Aerial roots (aer) is a tomato mutant characterized by the presence of numerous adventitious root primordia along the hypocotyl and older internodes. In this work, we have analyzed the aer mutant behavior to flooding to determine whether preformed adventitious roots represent an adaptive advantage with respect to biomass accumulation. We have also examined other morphological and anatomical responses of aer plants to detect differential adaptations under flooding. Aer plants form an abundant adventitious root system faster than Ailsa Craig cultivar, which results in flooded plants accumulating as much biomass as non-flooded aer plants. In addition, several ethylene-induced responses such as epinasty, hypertrophy, aerenchyma production, and apical hook formation are reduced in aer, suggesting a lower sensitivity of some tissues to ethylene. The E4 expression level, an ethylene-induced gene, confirmed this observation since E4 transcripts are less abundant in petioles and stems of ethylene-treated aer plants, coinciding with the tissues that present a lower degree of morphological and/or anatomical response. Evidence from the Never ripe mutant suggests a reduction in ethylene sensitivity could contribute to the attenuation of flooding effects. Therefore, our results indicate that the rapid formation of a new root system together with a reduction in ethylene sensitivity is responsible of a faster adaptation to flooding stress in the aer mutant.