Arabidopsis phospholipid modifications mediate cellulase-induced resistance to a fungal peptide antibiotic by imposing cell polarity

Plant-symbiotic Trichoderma fungi attack microorganisms by secreting antibiotic membrane-permeabilising peptaibols such as alamethicin. These peptaibols also permeabilise plant root epidermis plasma membranes (PMs), but mild pretreatment with Trichoderma cellulase activates a unique cellulase-induced resistance to alamethicin (CIRA), via an unknown mechanism. We identify two Arabidopsis genes that are essential for the CIRA process: CIRA12 encodes a phosphatidylserine (PS) decarboxylase and CIRA13, a phospholipase D zeta, implying that specific changes in anionic membrane lipids mediate alamethicin resistance. Fluorescent sensors revealed that cellulase induced a laterally asymmetric decrease in PS and surface charge to outer periclinal root epidermal PMs. Consistently, the CIRA response was reversed by addition of lysoPS. CIRA13 is essential for vesicle trafficking, which in turn is crucial for CIRA induction. Overall, cellulase induces a cellular polarity with respect to phospholipids, not previously observed in plants, that is leading to increased lipid packing and preventing peptaibol permeabilization of the outer periclinal membrane.