Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana

Abstract

Although aquaporins have been known to transport hydrogen peroxide (H(2)O(2)) across cell membranes, the H(2)O(2)-regulated expression patterns and the permeability of every family member of the plasma membrane intrinsic protein (PIP) toward H(2)O(2) have not been determined. This study investigates the H(2)O(2)-regulated expression levels of all plasma membrane aquaporins of Arabidopsis thaliana (AtPIPs), and determines the permeability of every AtPIP for H(2)O(2) in yeast. Hydrogen peroxide treatment of Arabidopsis down-regulated the expression of AtPIP2 subfamily in roots but not in leaves, whereas the expression of AtPIP1 subfamily was not affected by H(2)O(2) treatment. The growth and survival of yeast cells that expressed AtPIP2;2, AtPIP2;4, AtPIP2;5, or AtPIP2;7 was reduced in the presence of H(2)O(2), while the growth of yeast cells expressing any other AtPIP family member was not affected by H(2)O(2). These results show that only certain isoforms of AtPIPs whose expression is regulated by H(2)O(2) treatment are permeable for H(2)O(2) in yeast cells, and suggest that the integrated regulation of aquaporin expression by H(2)O(2) and the capacity of individual aquaporin to transport H(2)O(2) are important for plant response to H(2)O(2).

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

“…In addition to AtPIP1;4, five AtPIP2 isoforms (AtPIP2;1, AtPIP2;2, AtPIP2;4, AtPIP2;5, and AtPIP2;7) also were shown to increase H 2 O 2 sensitivity and decrease the viability of yeast under the de novo expression condition (Dynowski et al, 2008;Hooijmaijers et al, 2012 (Hooijmaijers et al, 2012). It was proposed that H 2 O 2 treatment of Arabidopsis reduced the expression of AtPIP2s in roots but not in leaves, while the expression of AtPIP1s was not affected.…”

“…It was further proposed that de novo expression of AtPIP2;2, AtPIP2;4, AtPIP2;5, or AtPIP2;7, but not AtPIP1s, impaired yeast growth and survival. However, de novo expression of AtPIP1;4 also was able to reduce yeast viability in response to 1 mM H 2 O 2 (Hooijmaijers et al, 2012). To date, the most convincing candidate in the PIP2 channel for H 2 O 2 transport is AtPIP2;1, the only PIP2 ortholog that has been demonstrated to increase H 2 O 2 uptake by yeast cells (Dynowski et al, 2008;Bienert and Chaumont, 2014).…”

“…To date, five AtPIP2 isoforms (AtPIP2;1, AtPIP2;2, AtPIP2;4, AtPIP2;5, and AtPIP2;7) have been assumed to mediate H 2 O 2 transport in engineered yeast cells (Bienert and Chaumont, 2014). Under de novo expression, these PIPs are able to increase H 2 O 2 sensitivity and decrease the viability of yeast (Dynowski et al, 2008;Hooijmaijers et al, 2012). However, only AtPIP2;1 has been elucidated to increase H 2 O 2 uptake by yeast cells (Dynowski et al, 2008;Bienert and Chaumont, 2014).…”

Reactive Oxygen Species in the Regulation of Stomatal Movements

“…Another model for recognition of apoplastic ROS signal assumes intracellular perception of apoplastic H 2 O 2 upon import through aquaporins. Indeed, the H 2 O 2 transport by plant aquaporins has been demonstrated in yeast cells (Bienert et al, 2007;Hooijmaijers et al, 2012), and a recent study by Tian et al (2016) provided evidence for occurrence of such events in planta. Finally, the apoplastic ROS could directly affect the activity of ion channels leading to stomatal closure.…”

ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants

“…For example, after the initial extracellular ROS production has elicited rapid ion fluxes to the cytosol and the triggering of responses in adjacent cells, a slower entry of extracellular ROS to the cell (e.g. through aquaporins; Hooijmaijers et al, 2012) could lead to inactivation of important amplification components (such as TPC1; Pottosin et al, 2009) and so termination of the signal in that cell. The prior propagation to adjacent cells would then lead to a wave-like rise-and-fall cell-to-cell progression of the Ca 2+ change.…”