Plant Aquaporin AtPIP1;4 Links Apoplastic H₂O₂ Induction to Disease Immunity Pathways

• Published in: Plant physiology (Bethesda) 2016-07, Vol.171 (3), p.1635-1650
• Main Authors: Tian, Shan, Wang, Xiaobing, Li, Ping, Wang, Hao, Ji, Hongtao, Xie, Junyi, Qiu, Qinglei, Shen, Dan, Dong, Hansong
• Format: Article
• Language: English
• Subjects: Aquaporins - genetics; Aquaporins - metabolism; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - microbiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Biological Transport - drug effects; Cell Membrane - metabolism; Disease Resistance - immunology; Gene Expression Regulation, Plant; Hydrogen Peroxide - metabolism; Hydrogen Peroxide - pharmacology; Nicotiana - genetics; Pathogen-Associated Molecular Pattern Molecules; Plant Diseases - immunology; Plant Immunity; Plants, Genetically Modified; Pseudomonas syringae - pathogenicity; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.15.01237

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 (PAMPs). This production of H₂O₂ 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 H₂O₂ production and functional performance. Expression of the AtPIP1;4 gene in plant leaves is inducible by a bacterial pathogen, and the expression accompanies H₂O₂ accumulation in the cytoplasm. Under de novo expression conditions, AtPIP1;4 is able to mediate the translocation of externally applied H₂O₂ into the cytoplasm of yeast (Saccharomyces cerevisiae) cells. In plant cells treated with H₂O₂, AtPIP1;4 functions as an effective facilitator of H₂O₂ transport across plasma membranes and mediates the translocation of externally applied H₂O₂ from the apoplast to the cytoplasm. The H₂O₂-transport role of AtPIP1;4 is essentially required for the cytoplasmic import of apoplastic H₂O₂ induced by the bacterial pathogen and two typical PAMPs in the absence of induced production of intracellular H₂O₂. As a consequence, cytoplasmic H₂O₂ 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 H₂O₂ but also cancels the subsequent immune responses, suggesting a pivotal role of AtPIP1;4 in apocytoplastic signal transduction in immunity pathways.