Review
Aquaporin structure–function relationships: Water flow through plant living cells

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Abstract

Plant aquaporins play an important role in water uptake and movement—an aquaporin that opens and closes a gate that regulates water movement in and out of cells. Some plant aquaporins also play an important role in response to water stress. Since their discovery, advancing knowledge of their structures and properties led to an understanding of the basic features of the water transport mechanism and increased illumination to water relations. Meanwhile, molecular and functional characterization of aquaporins has revealed the significance of their regulation in response to the adverse environments such as salinity and drought. This paper reviews the structure, species diversity, physiology function, regulation of plant aquaporins, and the relations between environmental factors and plant aquaporins. Complete understanding of aquaporin function and regulation is to integrate those mechanisms in time and space and to well regulate the permeation of water across biological membranes under changing environmental and developmental conditions.

Introduction

The discovery of aquaporins showed a new insight into the mechanism of water-transmembrane transportation (the model in Fig. 1), which provided solid molecular basis for fast and reversible regulation of transmembrane water transport and gave strong support to the idea that such high water permeability might be required for certain physiological processes [1], [2]. Aquaporins, or major intrinsic proteins (MIPs), are channel-forming membrane proteins with the extraordinary ability to combine a high flux with a high specificity for water across biological membranes. They belong to a well-conserved and ancient family of proteins called the major intrinsic proteins (MIPS) with molecular weights in the range of 26–34 kDa [3], with members found in nearly all living organisms. The aquaporin family in plants is large, indicating complex and regulated water transport within the plant in order to adapt to different environmental conditions, which includes more than 150 membrane channel proteins [4]. Regulation of aquaporin-mediated water flow, through indirect or direct means, appears to be a mechanism by which plants can control cellular and tissue water movement [5]. All aquaporin isoforms probably work together in an orchestrated manner, where each individual aquaporin isoform displays a specific localization pattern, substrate specificity, and regulatory mechanism [6]. The structure, function and gene regulation of aquaporins as well as research methodology are reviewed as following.

Section snippets

Diversity of plant aquaporins

The physiological role of water channel proteins is particularly important in plants because of their continuous water recruitment [7], [8]. Many more MIP family genes have since been identified in plants, with additional members in Arabidopsis, tobacco, spinach, tomato, the ice plant (Mesembryanthemum crystallinum), radish, and snapdragon [2], [3], [9]. The permeability values establish limits on aquaporin tissue densities required for physiological function and suggest significant structural

Aquaporin gene expression and diurnal fluctuations

Because of aquaporin potentially important role in regulating water flow in plants, studies documenting aquaporin gene expression in specialized tissues involved in water and solute transport are important [35], [36]. The high level of expression of ZmTIP1 in maize tissues (root epidermis, root endodermis, small parenchyma cells surrounding mature xylem vessels in the root, and so on) facilitates rapid flow of water through the tonoplast to permit osmotic equilibration between the cytosol and

Aquaporin cellular and subcellular localization

Regardless of whether all or only the majority of the plant MIPs are aquaporins, it is clear that a large number of aquaporins are present in plants, some localized in the tonoplast, some in the plasma membrane and some possibly localized in endomembranes [4], [6], [11], [18], [20], [21], [26], [32], [45]. MIP-B was found in fractions containing tonoplast proteins and possibly in a fraction of intermediate density, distinct from both plasma membrane and tonoplast, and also distinct from the

Aquaporin structure and selectivity

The structure of aquaporins is highly conserved in animals, plants, yeast, and bacteria [4]. All MIP family proteins share six putative transmembrane domains with the N- and C-termini facing the cytosol (Fig. 2). The six transmembrane domains were predicted to be α-helices, packed together with the pore-forming domains outside and towards the center of an aquaporin tetramer [4], [26], [28], [56]. There are five loops (A–E) joining the transmembrane helices. The first cytosolic loop and the

Change and regulation of aquaporin water permeability

Land plants have evolved to cope with rapid changes in the availability of water by regulating all aquaporins that lie within the plasma membrane [1]. Regulation of aquaporin trafficking may also represent a way to modulate membrane water permeability, and the factors affecting and regulating aquaporin behaviors possibly involve phosphorylation, heteromerization, pH, Ca2+, pressure, solute gradients and temperature drought, flooding and so on (Fig. 3), which suggests aquaporins are involved in

Conclusions and future perspectives

The discovery of aquaporins in plants has resulted in a paradigm shift in the understanding of plant water relations. Water flux across cell membranes has been shown to occur not only through the lipid bilayer, but also through aquaporins, which are members of the major intrinsic protein super-family of channel proteins [2], [3], [5], [9], [20], [32]. As has been found in other organisms, plant MIPs function as membrane channels permeable to water (aquaporins) and in some cases to small

Acknowledgements

Research in Professor Shao HB's laboratory is jointly supported by the foundation from Doctoral Foundation of QUST (0022221),and Qingdao Agricultural University 630523, Shao Ming-An's Innovation Team Project of Education Ministry of China and Northwest A&F University, and Specialized Initiation Foundation of Excellent Ph.D. Dissertation of Chinese Academy of Sciences.

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    Shao Hong-Bo and Zhao Chang-Xing is the Co-first author for this article.

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