Aquaporin as a membrane transporter of hydrogen peroxide in plant response to stresses

Abstract

Hydrogen peroxide (H₂O₂) is a reactive oxygen species that signals between cells, and H₂O₂ signaling is essential for diverse cellular processes, including stress response, defense against pathogens, and the regulation of programmed cell death in plants. Although plasma membrane intrinsic proteins (PIPs) have been known to transport H₂O₂ across cell membranes, the permeability of each family member of PIPs toward H₂O₂ has not yet been determined in most plant species. In a recent study, we showed that certain isoforms of Arabidopsis thaliana AtPIPs, including AtPIP2;2, AtPIP2;4, AtPIP2;5, and AtPIP2;7, are permeable for H₂O₂ in yeast cells. Since the expression of PIPs is differently modulated in Arabidopsis by abiotic stress or H₂O₂ treatment, it is important to investigate the integrated regulation of aquaporin expression and their physiological significance in H₂O₂ transport and plant response to diverse abiotic stresses.

The functional roles of hydrogen peroxide (H₂O₂) as a signaling and regulatory molecule have been implicated in many cellular processes, including photosynthesis, photorespiration, stomatal movement, cell cycle, senescence, and stress response.¹ The effect of H₂O₂ in these cellular processes requires a rapid transport of the intercellular messenger molecule across the plasma membrane. Although H₂O₂ can diffuse across cell membranes, native membranes represent significant barriers against H₂O₂, and many membranes are poorly permeable to H₂O₂.² Because efficient transport of H₂O₂ across plasma membranes can be greatly increased by specific channel proteins, it is important to determine which channel proteins can facilitate H₂O₂ transport across plasma membranes.

The major intrinsic proteins (MIPs), commonly referred to as aquaporins, have been determined to facilitate the transport not only of water but also other substrates, including glycerol, ammonia, urea, boric acid, carbon dioxide, nitric oxide, and lactic acid.^3,4 Although several studies have demonstrated that certain aquaporins facilitate the diffusion of H₂O₂ across biological membranes,^5,6 reports demonstrating the permeability of plasma membrane intrinsic proteins (PIPs) toward H₂O₂ are severely limited. In a recent study, we showed that certain isoforms of Arabidopsis thaliana AtPIPs, including AtPIP2;2, AtPIP2;4, AtPIP2;5, and AtPIP2;7, are permeable for H₂O₂ in yeast cells.⁷

With the increasing understanding of the capacity of aquaporins to facilitate the transport of H₂O₂ across plasma membranes and the involvement of H₂O₂ in plant response to abiotic stresses, it is of interest to investigate the physiological significance of aquaporin-mediated H₂O₂ transport in plants under stress conditions. It has been suggested that abiotic and biotic stress-related stimuli mediated an H₂O₂-induced internalization of PIPs to downregulate root water transport.⁸ It has been reported that exogenously applied H₂O₂ to the roots of cucumber, wheat, maize, and bean affected the hydraulic conductivity under normal or stress conditions.^9-12 The comprehensive expression patterns of AtPIPs have been analyzed in Arabidopsis under environmental stresses, including cold, salt, and drought.¹³ In a recent study, we showed that hydrogen peroxide treatment did not affect the endogenous expression levels of AtPIP1 in the leaves and roots of Arabidopsis, whereas AtPIP2 genes, including AtPIP2;2, AtPIP2;3, AtPIP2;4, AtPIP2;5, and AtPIP2;7, in the roots were downregulated by H₂O₂ treatment.⁷ The integrated regulation of AtPIPs expression by H₂O₂ or abiotic stresses is summarized in Figure 1. The expression of AtPIP2;2, AtPIP2;4, AtPIP2;5, and AtPIP2;7, which are permeable for H₂O₂ in yeast cells, was differently modulated by abiotic stresses. In particular, the expression of AtPIP2;2, AtPIP2;4, and AtPIP2;7 was downregulated by both H₂O₂ and drought stress (Fig. 1). The concomitant regulation in the expression of certain aquaporin family members by H₂O₂ and abiotic stresses suggests that these specific members of aquaporin may play an important role in H₂O₂-mediated plant response to changing environmental conditions. Further researches should focus on determining the physiological consequence of aquaporin-mediated H₂O₂ transport in plant adaptation to diverse abiotic stresses.

Figure 1. Summary of the involvement of the Arabidopsis AtPIPs in H₂O₂ and abiotic stress responses. The expression patterns reported in Hooijmaijers and Jang^7,13 were used to group the AtPIP genes based on their H₂O₂ or stress responses, and the arrows indicate the genes that are upregulated or downregulated by the indicated treatments in the aerial parts and roots of Arabidopsis plants. The numbers 1;1, 1;2, 1;3, etc., in the figure represent AtPIP1;1, AtPIP1;2, AtPIP1;3, etc., respectively, and the red colors represent the AtPIPs that are permeable for H₂O₂ in yeast cells.

Glossary

Abbreviations:

MIP

major intrinsic protein

PIP

plasma membrane intrinsic protein

Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, et al. Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res. 2012;125:147–53. doi: 10.1007/s10265-011-0413-2.