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Front. Plant Sci., 09 June 2017 | https://doi.org/10.3389/fpls.2017.01018

Multifunctional Roles of Plant Dehydrins in Response to Environmental Stresses

  • State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an, China

To respond to environmental changes, plants have developed complex mechanisms that allow them to rapidly perceive and respond to abiotic stresses. Late embryogenesis abundant (LEA) proteins are a large and diverse family that play important roles in environmental stress tolerance in plants. Dehydrins belong to group II LEA proteins, which are considered stress proteins involved in the formation of plants’ protective reactions to dehydration. Some studies have demonstrated that dehydrins could binding metal ions or lipid vesicles. In vitro experiments revealed that dehydrins could protect the activity of enzyme from damage caused by environmental stress. Although many studies have been conducted to understand their roles in abiotic stresses, the molecular function of dehydrins is still unclear. In this review, to generate new ideas for elucidating dehydrins’ functions, we highlight the functional characteristics of dehydrins to understand their roles under environmental stress in plants.

Introduction

Late embryogenesis abundant (LEA) proteins are related with the acquisition of desiccation tolerance in plants and are accumulated during the late stages of seed development (Dure and Galau, 1981; Liu et al., 2013, 2016). According to the conserved segments, LEA proteins can be categorized into seven different groups (Battaglia et al., 2008). Dehydrins belong to the group II LEA proteins, which were initially identified as the “D-11" family in the developing cotton embryos. Dehydrins are considered stress proteins involved in the formation of plants’ protective reactions to dehydration. They can also be considered as hydrophilins. They are highly hydrophilic, containing a high proportion of charged and polar amino acids and a low fraction of hydrophobic, non-polar residues, and lack tryptophan and cysteine residues. Based on the presence of conserved sequences (Y-, S-, and K-segments), dehydrins were classified into the different sub-classes YnKn, YnSKn, KnS, SKn and Kn (Garay-Arroyo et al., 2000).

Although the function of dehydrins has not been clearly understood, many studies have demonstrated dehydrins play important roles in abiotic stress tolerance. Overexpression of the Prunus mume dehydrin PmLEAs in tobacco and Escherichia coli enhances tolerance to cold and drought (Bao et al., 2017). Overexpression of the Solanum habrochaites dehydrins ShDHN enhances transgenic tomato tolerance to multiple abiotic stresses (Liu et al., 2015). Most dehydrins are distributed along with several ubiquitous dehydration-stress response protein types in plants (Bao et al., 2017; Fan et al., 2017). However, some dehydrins were also found distributed in the vegetative tissues of plants grown under normal conditions, which suggested that the dehydrins may play important roles in the plant growth. Recently, studies indicate that the Medicago truncatula Y2K4-type dehydrin MtCAS31 could interact with AtICE1 (an inducer of CBF expression 1). The interaction of AtICE1with MtCAS31 plays important roles in stomatal development, enhancing the drought resistance by decreasing in stomatal density of transgenic Arabidopsis thaliana (Xie et al., 2012).

The Roles of the Different Conserved Segments in Dehydrins

The K-segment can form an amphiphilic α-helix, which representing a highly conserved 15 amino acid segment (EKKGIMDKIKEKLPG) that has been found in all dehydrins (Malik et al., 2017). The α-helix of dehydrins may help stabilize the proteins and the cellular membranes under environmental stress conditions. The Citrus unshiu K3S-type dehydrin CuCOR19 was found to form an α-helix in the presence of SDS (sodium dodecyl sulfate) (Hara et al., 2001). The K-segment of the maize dehydrin DHN1 is essential for binding to the anionic phospholipid vesicles, and the adoption of α-helicity by the K-segment accounts for the conformational change in dehydrins upon binding to SDS or anionic phospholipid vesicles (Koag et al., 2009). The K-segment of wheat dehydrin DHN-5 is required for the protection of β-glucosidase and LDH (lactate dehydrogenase) activities in vitro (Drira et al., 2013). The lysine-rich segment of the Craterostigma plantagineum disordered stress protein CDeT11-24 is important for the protection of proteins from damage caused by water stress and the phosphatidic acid (PA) binding (Petersen et al., 2012). The cold-induced dehydrin Lti30 can bind to cellular membranes via its K-segments, which locally fold into α-helix on the cellular membrane surface. The protein Lti30’s K-segments electrostatically trap the negatively charged lipid head (Eriksson et al., 2011, 2016).

The Y-segment, representing a conserved segment [V/T]D[E/Q]YGNP, is usually found in various tandem copies in the N-terminus of dehydrins (Campbell and Close, 1997). The Y-segment of dehydrins has sequence similarity to the nucleotide-binding site of plant and bacterial chaperones [(V/T) DEYGNP]. However, there is no experimental evidence suggesting that the Y-segment binds nucleotides (Close, 1996; Hughes et al., 2013).

Some dehydrins contain the S-segment, which consists of a tract of Ser residues and can be phosphorylated. The phosphorylation of the S-segment is suggested to promote dehydrins interaction with the specific signal peptides followed by their translocation into the nucleus (Goday et al., 1994; Close, 1996; Jiang and Wang, 2004). The S-segment can be phosphorylated by protein kinase, which may influence the location and the ability to bind metal ions (Goday et al., 1994; Alsheikh et al., 2003). The three amino acid residues EDD of the maize dehydrin Rab17 are the CKII phosphorylation recognition site (Jensen et al., 1998).

The Φ-segments are less conserved motifs, which lay interspersed between K-segments (Campbell and Close, 1997).

The Function of Dehydrins

Binding Metal Ions

Under control conditions, catalytic metal ions (such as Cu2+ and Zn2+) mainly exist as metal-protein complexes in plants. Nevertheless, they can be released as free ions when plants are subjected to stress conditions. These free ions are required to produce ROS (reactive oxygen species) via the Fenton or the Haber–Weiss reactions (Mittler, 2002). It has been reported that the Ricinus KS-type dehydrin ITP is the first member of the LEA protein family shown to be active in the long-distance transport micronutrients (Krüger et al., 2002). The Arabidopsis thaliana dehydrin AtHIRD11 and citrus dehydrin CuCOR15 can bind the metal ions Fe3+, Co2+, Ni2+, Cu2+ and Zn2+ over Mg2+and Ca2+ (Hara et al., 2005, 2011).

Binding DNA

The bioinformatic analysis of the “Protein or Oligonucleotide Probability Profile (POPP)” predicted that dehydrins could bind DNA (Wise and Tunnacliffe, 2004). Until now, several studies have reported that LEA protein can bind DNA. Citrus dehydrin CuCOR15 can bind nucleic acids, a process that depends on zinc ions. The histidine-rich domain (TTDVHHQQQYHGGEH) and the lysine-rich domain (GGEGAHGEEKKKKKKEKKK) were the DNA-binding domains (Hara et al., 2009). Y2K-type dehydrin VrDhn1 exhibited a low affinity for non-specific interaction with DNA, and the exogenous addition metal ions of Zn2+ or Ni2+ stimulated the interaction (Lin et al., 2012).

Binding Phospholipid

Phosphatidic acid is the important stress-signaling phospholipid, and its accumulation is triggered in response to various environmental stress conditions, such as salinity, drought and cold (Frank et al., 2000; Katagiri et al., 2005). The PA concentration in the turgescent plant membranes is only approximately 1%, but increases under water deficit stress. The formation of PA depends on the activity of phospholipase D, which can be induced by ABA and dehydration (Katagiri et al., 2001).

Many studies have demonstrated that dehydrin can bind with phospholipids, and the binding was not limited to a certain type of phospholipids (Kooijman et al., 2007; Koag et al., 2009; Petersen et al., 2012). The maize SK2- type dehydrin DHN1 can bind PA. Although most of the DHN1 protein is disorder, the K-segment can adopt α-helical conformation. An electrostatic nature of the interaction has been postulated. The basic amino acids, such as arginine and lysine, are required for the interaction in the binding domain (Kooijman et al., 2007; Koag et al., 2009). The Kn-type dehydrin Lti30 can interact electrostatically with vesicles of both negatively charged phospholipids (phosphatidic acid, phosphatidyl serine and phosphatidyl glycerol) and zwitterionic (phosphatidyl choline). The Lti30 interaction of lipid is regulated by phosphorylation, pH dependent His on/off switch, and the reversal of membrane binding by proteolytic digest (Eriksson et al., 2011).

Protecting the Activity of Proteins

The hypothesis that dehydrin can bind proteins to prevent its denaturation has been suggested for many years. Many studies have demonstrated that dehydrin can protect the activity of LDH and malate dehydrogenase from damage caused by various environmental stresses (Drira et al., 2013, 2015; Yang et al., 2015). The KS-type dehydrin AtHIRD11 recovers LDH activity inhibited by copper with the contribution of histidine residues (Hara et al., 2016). However, the interaction between the dehydrins and the protected proteins has been not found.

Scavenging the Reactive Oxygen Species

Many studies have indicated that dehydrins can directly scavenge the free radicals. The citrus dehydrin CuCOR19 displays a stronger inhibition against free radical-inducing peroxidation. The overexpression CuCOR19 in transgenic tobacco can inhibit lipid peroxidation under cold stress (Hara et al., 2003). The amino acids, such as histidine, lysine and glycine, are targets for radical-mediated oxidation (Dean et al., 1997). The content of the three amino acids is high in mostly dehydrins, which can reduce the level of ROS. The Arabidopsis thaliana KS-type dehydrin AtHIRD11 can reduce ROS generation from copper. The length of the peptides and the histidine contents are fundamental factors that can influence the ROS decrease by the KS-type dehydrins (Hara et al., 2013, 2016).

Conclusion

To summarize the data presented above, the functional mechanisms are listed as follows.

(I) Dehydrins can bind metal ions, which can inhibit the production of ROS at the source.

(II) The high content of the antioxidant amino acids, such as lysine, histidine and glycine, can scavenge ROS through oxidative modification.

(III) Dehydrins can non-specifically bind proteins and membranes, which can protect the function and structure of the protein or membrane from damage caused by environmental stresses.

(IV) Dehydrins can bind DNA, which may repair or protect the DNA from damage caused by environmental stresses.

Author Contributions

YL wrote the article. QS and DaL gave positive suggestion about this article. DeL and XY revised the paper and gave positive suggestion. All authors read and approved the manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This work was supported by the Shandong Province Natural Science Foundation (ZR2016CQ34) and the Grants from the Nation Natural Science Foundation of China (Nos. 31271633).

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Keywords: dehydrin, conserved segments, LEA protein, abiotic stresses, function

Citation: Liu Y, Song Q, Li D, Yang X and Li D (2017) Multifunctional Roles of Plant Dehydrins in Response to Environmental Stresses. Front. Plant Sci. 8:1018. doi: 10.3389/fpls.2017.01018

Received: 14 March 2017; Accepted: 29 May 2017;
Published: 09 June 2017.

Edited by:

Sergio J. Ochatt, INRA - UMR 1347 Agroécologie, France

Reviewed by:

Fisun G. Çelikel, Ondokuz Mayıs University, Turkey
Khawar Jabran, Duzce University, Turkey

Copyright © 2017 Liu, Song, Li, Yang and Li. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Dequan Li, dqli@sdau.edu.cn Xinghong Yang, xhyang@sdau.edu.cn