NAC-mediated membrane lipid remodeling negatively regulates fruit cold tolerance

Abstract

Low temperatures are known to destroy cell membranes' structural integrity by affecting the remodeling of their phospholipids. Fruits stored at low temperature are prone to chilling injury, characterized by discoloration, absence of ripening, surface pitting, growth inhibition, flavor loss, decay, and wilting. Phosphatidic acid, a vital second-messenger lipid in plants, is known to accumulate in response to different kinds of stress stimuli. However, the regulatory mechanism of its production from the degradation of phospholipids remains poorly understood. We identified two cold-responsive NAC (NAM/ATAF1/CUC2) transcription factors from bananas, namely, MaNAC25 and MaNAC28, which negatively regulated cold tolerance in banana fruits by upregulating the expression of phospholipid degradation genes in banana fruits. Furthermore, MaNAC25 and MaNAC28 formed a positive feedback loop to induce phospholipid degradation and produce phosphatidic acid. In contrast, ethylene directly inhibited the degradation of phospholipids in banana and transgenic tomato fruits. In addition, ethylene reduced the activity of MaNAC25 and MaNAC28, thereby inhibiting phospholipid degradation. To conclude, NAC-mediated membrane lipid remodeling negatively regulates the cold tolerance of banana and transgenic tomato fruits.