Plant Aquaporin AtPIP1;4 Links Apoplastic H2O2 Induction to Disease Immunity Pathways1[OPEN]

The plasma membrane aquaporin AtPIP1;4 facilitates the diffusion of pathogen-induced apoplastic H 2 O 2 to activate plant immunity. Hydrogen peroxide (H2O2) is a stable component of reactive oxygen species, and its production in plants represents the successful recognition of pathogen infection and pathogen-associated molecular patterns ( PAMP s). This production of H 2 O 2 is typically apoplastic but is subsequently associated with intracellular immunity pathways that regulate disease resistance, such as systemic acquired resistance and PAMP -triggered immunity. Here, we elucidate that an Arabidopsis ( Arabidopsis thaliana ) aquaporin (i.e. the plasma membrane intrinsic protein AtPIP1;4) acts to close the cytological distance between H 2 O 2 production and functional performance. Expression of the AtPIP1;4 gene in plant leaves is inducible by a bacterial pathogen, and the expression accompanies H 2 O 2 accumulation in the cytoplasm. Under de novo expression conditions, AtPIP1;4 is able to mediate the translocation of externally applied H 2 O 2 into the cytoplasm of yeast ( Saccharomyces cerevisiae ) cells. In plant cells treated with H 2 O 2 , AtPIP1;4 functions as an effective facilitator of H 2 O 2 transport across plasma membranes and mediates the translocation of externally applied H 2 O 2 from the apoplast to the cytoplasm. The H 2 O 2 -transport role of AtPIP1;4 is essentially required for the cytoplasmic import of apoplastic H 2 O 2 induced by the bacterial pathogen and two typical PAMP s in the absence of induced production of intracellular H 2 O 2 . As a consequence, cytoplasmic H 2 O 2 quantities increase substantially while systemic acquired resistance and PAMP -triggered immunity are activated to repress the bacterial pathogenicity. By contrast, loss-of-function mutation at the AtPIP1;4 gene locus not only nullifies the cytoplasmic import of pathogen- and PAMP -induced apoplastic H 2 O 2 but also cancels the subsequent immune responses, suggesting a pivotal role of AtPIP1;4 in apocytoplastic signal transduction in immunity pathways.