Responses and tolerance to salt stress in bryophytes

Abstract

During exposure to salt environments, plants could perceive salt signal and transmit the signal to cellular machinery to activate adaptive responses. In bryophytes, salt signal components and transcript factor identified suggest that salt activate adaptive responses to tolerate adverse environments. The ability of bryophytes to tolerate salt is determined by multiple biochemical pathways. Transmembrane transport proteins that mediate ion fluxes play a curial role in ionic and osmotic homeostasis under salt environments. Defense proteins protect cells from denaturation and degradation, as well as from oxidative damage following exposure to salt stress in bryophytes. ABA and salt stress positively affect the expression of common genes that participate in protection plant cells from injure, and ABA may be responsible for the ability to tolerate salt stress in bryophytes. In this paper, we reveal the mechanisms of salt responses and tolerance in bryophytes, and imply conservation between higher plants and bryophytes in response and tolerance to salt stress.

Introduction

Due to their sessile nature, plants have to endure adverse environmental conditions such as soil salinity. Excess salts in the soil inhibit plant growth and cause great losses in agricultural productivity worldwide.1 Therefore, understanding the mechanisms by which plants perceive salt signal and transmit the signal to cellular machinery to active adaptive responses is of fundamental importance to biology. The responses of higher plants to salt stress have been studies intensively at the cellular and molecular levels as well as at the physiological and biochemical levels.2 However, little is known about the mechanisms underlying salt responses and tolerance in bryophytes.

Bryophytes are well known because of their importance in the study of plant systematics and evolution, as well as the tolerance of harsh environments.3 This review focuses on the responses and tolerance of salt stress in bryophytes. These processes include signal transduction, transcript regulation, ionic and osmotic homeostasis, biosynthesis defense proteins, and the roles of phytohormone in salt stress. Our article will provide the complex mechanisms of salt responses and tolerance in bryophytes.

Salt Signal Compoments and Transcript Regulation

Molecular and proteomic analyses have shown that several different signal components and transcriptional regulator are involved in salt stress responses. These proteins are phototropin, myelin basic protein kinase, MCamb1 and MCamb2, 14-3-3 like protein and PpDBF1.4–7

Phototropin is the blue light receptor that mediates phototropism, chloroplast relocation and stomatal opening in higher plants.8 In Physcomitrell patens, phototropin and 14-3-3 proteins may work cooperatively to regulate plasma membrane H⁺-ATPase and maintain ion homeostasis.4 The 14-3-3 proteins are important eukaryotic regulatory proteins, most of which are involved in cellular signaling pathways.9 Through regulating the activities of kinases and phosphatase, 14-3-3 proteins integrate themselves into several levels of signal transduction cascades.10–12 Protein kinases play a central role in signal transduction events in organisms. In Funaria hygrometrica, salt could activate the myelin basic protein kinase, which belongs to stress-activated protein kinases.5 Plants responses to environmental stresses are mediated in part by signaling processes involving cytosolic Ca²⁺ and a Ca²⁺-binding protein, calmodulin. MCamb1 and MCamb2 are novel membrane transporter-like proteins identified in P. patens and they bind to calmodulin via interaction with basic amphiphilic amino acids in the C-terminal domain. The finding of salt-inducible gene expression of MCamb1 and MCamb2 in P. patens indicates that Ca²⁺ might play a role in signaling events leading to the development of stress resistance through modulation of stress-inducible CaM-binding membrane transporters in bryophytes.6

Transcriptional control is a major mechanism whereby a cell or organism regulates its gene expression. Sequence-specific DNA-binding transcriptional regulators, one class of transcription factors, play an essential role in modulating the rate of transcription of specific target genes.13 DREB transcription factors that bind to dehydration responsive elements (DRE) or C-repeat elements (CRT) belong to the large family of AP2/ERF transcription factors.14 They play critical roles in regulating expression of stress-inducible genes under abiotic stresses in higher plants.14,15 A DREB homolog, PpDBF1, has been isolated from P. patens. PpDBF1 transcript has been activated by salt stress in P. patens. These have shown that PpDBF1 may play a role in P. patens as a DREB transcription factor, and also imply that similar regulating systems are conserved in bryophytes and higher plants.7

Modulation of Ionic and Osmotic Homeostasis

Ion uptake and compartmentalization are crucial for the growth of plants under both normal and salt conditions. High apoplastic levels of Na⁺ and C1⁻ alter the aqueous and ionic thermodynamic equilibrium resulting in hyperosmotic stress, ionic imbalance and toxicity. Thus, it is vital for the plant to re-establish cellular ion homeostasis in salt environments. Ion homeostasis in salt environments of bryophytes is dependent on transmembrane transport proteins that mediate ion fluxes, including sodium ATPase (PpENA1 and PpENA2), vacuolar H⁺-ATPase, PpSHP1 and PpSHP2, chloride channel protein and ABC transporters.4,16–18

Na⁺ competes with K⁺ for intracellular influx because these cations are transported by common proteins.19,20 During exposure to salt environments, the maintenance of K⁺ and Na⁺ homeostasis is crucial in organisms. The H⁺-ATPase and Na⁺-ATPase are thus proteins that could meditate Na⁺ efflux and K⁺ influx into cells. Na⁺-ATPase has existed in early land plants but that they are lost during the evolution of bryophytes to flowering plants. PpSHP1 and PpSHP2 share a high degree of sequence homology with PMP3 gene from yeast and RCI gene from Arabidopsis.18 Those proteins may be involved in the salt responses by avoiding over-accumulation of Na⁺ and K⁺ ions.18,21 Chloride interferes with anionic sites involved in the binding of RNA and sugar-phosphates.22,23 Downregulation of the chloride channel protein limits the transport of Cl⁻ into the cells.4 In addition, ABC transporters may also be involved in the regulation of homeostasis in bryophytes.4

Biosynthesis Defense Proteins

In general, stress results in mis-folding or unfolding of proteins, which is harmful to the cell. HSP70 is responsible for protecting proteins from denaturation and degradation during salt stress in P. patens.4 Generation of ROS is a common phenomenon in plants during stress. ROS disrupt normal metabolism via oxidative damage to lipids, proteins and nucleic acids. The antioxidative enzymes, such as cytochrome P450 monooxygenase, LOXs, 2-Cys peroxiredoxin and peroxiredoxin, play a crucial role in protecting cells from oxidative damage during salt stress in P. patens.4 In addition, salt induces the expression of several defense genes that encode the proteins of group II LEA and group III LEA, PpCOR47, PpCOR TMC-AP3 and WCOR413 cold-acclimation protein.24–26 LEA proteins, a class of protein originally identified in seeds during the later stages of embryogenesis, could improve or protect enzyme activity; or act as radical scavengers or as membrane stabilizers.27 COR proteins have roles in freezing tolerance, and it is interest that many COR proteins are induced in response to drought, osmotic, salt and ABA treatment.25

Roles of ABA in Salt Tolerance

In higher plants, the phytohormone abscisic acid (ABA) plays a major role in seed maturation and germination, as well as in adaptation to environmental stresses. In bryophytes, the roles of ABA has been described with respect to their ability to tolerate severe desiccation and freezing environment.28–31 Endogenous ABA levels are dramatically increased by dehydration in Exormotheca holstii, Funaria hygrometrica and Riccia fluitans.29–31 In comparison to the studies on desiccation and freezing tolerance, information on the salt tolerance of bryophytes is quite limited. Most research has been concentrated on the gene expression of exposure to both exogenous ABA and salt conditions. These ABA- and salt-responsive genes encode a variety of proteins, such as ALDH 21A1, ALDH7B6, COR47, COR TMC-AP3, WCOR413 cold-acclimation protein, group II LEA and group III LEA proteins, myelin basic protein kinase, MCamb1 and MCamb2, PpDBF1, PpSHP1 and PpSHP2.5–7,18,24–26,32,33 Thus it can be seen that ABA and salt stress positively affect the expression of common genes that participate in protection plant cells from injure. It also suggests that ABA may be responsible for the ability to tolerate salt stress in bryophytes.

Conclusion

Bryophytes are one of the earliest land plants in evolutionary terms, and make significant contributions to understanding of the development, physiology, phylogenetics and stress-induced cellular responses of plants. In this review, we expatiate that the complex mechanisms of salt responses and tolerance in bryophytes, and imply that similar responsive systems are conserved in bryophytes and higher plants. However, the responsive mechanisms have largely remained a mystery until recently, and we are still far from having a clear picture. Therefore, in order to make a better understanding the salt responsive mechanisms in bryophytes, the challenge in the near future remains to identify more salt responsive elements.

Abbreviations

ABC	=	ATP-binding cassette
ALDH	=	aldehyde dehydrogenase
COR	=	cold regulated
HSP	=	hot shock protein
LEA protein	=	later stages of embryogenesis protein
LOXs	=	lipoxygenases
MCamb	=	calmodulin-binding proteins
PpDBF	=	Physcomitrella patens DRE-binding factor
PpSHP	=	Physcomitrella patens small hydrophobic protein
ROS	=	reactive oxygen species

Acknowledgements

This work was supported by grants from Beijing National Science Key Foundation (KZ20061002817 and 5021001), Chinese 863 Project (2007AA021405), and the Institutions of Higher Learning under the Jurisdiction of the Beijing Municipality for Academic Human Resources Development to He.