▪ Abstract Plant responses to salinity stress are reviewed with emphasis on molecular mechanisms of signal transduction and on the physiological consequences of altered gene expression that affect biochemical reactions downstream of stress sensing. We make extensive use of comparisons with model organisms, halophytic plants, and yeast, which provide a paradigm for many responses to salinity exhibited by stress-sensitive plants. Among biochemical responses, we emphasize osmolyte biosynthesis and function, water flux control, and membrane transport of ions for maintenance and re-establishment of homeostasis. The advances in understanding the effectiveness of stress responses, and distinctions between pathology and adaptive advantage, are increasingly based on transgenic plant and mutant analyses, in particular the analysis of Arabidopsis mutants defective in elements of stress signal transduction pathways. We summarize evidence for plant stress signaling systems, some of which have components analogous to t...

Plant cellular and molecular responses to high salinity.

Halophytes, plants that survive to reproduce in environments where the salt concentration is around 200 mM NaCl or more, constitute about 1% of the worlds flora. Some halophytes show optimal growth in saline conditions; others grow optimally in the absence of salt. However, the tolerance of all halophytes to salinity relies on controlled uptake and compartmentalization of Na+, K+ and Cl- and the synthesis of organic compatible solutes, even where salt glands are operative. Although there is evidence that different species may utilize different transporters in their accumulation of Na+, in general little is known of the proteins and regulatory networks involved. Consequently, it is not yet possible to assign molecular mechanisms to apparent differences in rates of Na+ and Cl- uptake, in root-to-shoot transport (xylem loading and retrieval), or in net selectivity for K+ over Na+. At the cellular level, H+-ATPases in the plasma membrane and tonoplast, as well as the tonoplast H+-PPiase, provide the transmembrane proton motive force used by various secondary transporters. The widespread occurrence, taxonomically, of halophytes and the general paucity of information on the molecular regulation of tolerance mechanisms persuade us that research should be concentrated on a number of model species that are representative of the various mechanisms that might be involved in tolerance.

Salinity tolerance in halophytes

In many plants, free proline accumulates in response to the imposition of a wide range of biotic and abiotic stresses. Controversy has surrounded the extent to which this shift in nitrogen metabolism benefits plants under adverse environmental conditions. Most attempts to account for the phenomenon have focused on the ability of proline to mediate osmotic adjustment, stabilise subcellular structures and scavenge free radicals. However, often the cytoplasmic pool of free proline even after the imposition of stress is insufficient size to account for pronounced biophysical effects. Alternatively, selective preservation of this stress-induced response may relate to endpoints other than simply augmenting the cellular pool of free proline. Proline accumulation may reduce stress-induced cellular acidification or prime oxidative respiration to provide energy needed for recovery. High levels of proline synthesis during stress may maintain NAD(P)+/NAD(P)H ratios at values compatible with metabolism under normal conditions. Consideration of the cofactor preference of plant Δ1-pyrroline-5-carboxylate (P5C) reductase as well as the in vivo concentrations of the two pyridine nucleotide cofactors and their respective redox ratios suggests that even a small increase in proline biosynthesis might have a large impact on the level of reduction of the cellular NADP pool. The increased NADP+/NADPH ratio mediated by proline biosynthesis is likely to enhance activity of the oxidative pentose phosphate pathway. This would provide precursors to support the demand for increased secondary metabolite production during stress as well as nucleotide synthesis accompanying the accelerated rate of cell division upon relief from stress, when oxidation of proline is likely to provide an important energy source for ADP phosphorylation. Thus, the extreme sensitivity of the metabolic processes of proline synthesis and degradation themselves may be of benefit by regulating metabolic processes adversely affected by stress. This viewpoint is supported by consideration of other physiological phenomena not directly related to stress responses, but in which proline metabolism may also play a regulatory role. A mechanism is proposed whereby the interconversions of proline and P5C in different cell types and the associated transfer of redox potential between tissues may constitute a form of metabolic signalling within higher plants. Stress-related alterations in proline metabolism may impinge on systems of redox control of plant gene expression.

Metabolic implications of stress-induced proline accumulation in plants

Many plants accumulate organic osmolytes in response to the imposition of environmental stresses that cause cellular dehydration. Although an adaptive role for these compounds in mediating osmotic adjustment and protecting subcellular structure has become a central dogma in stress physiology, the evidence in favour of this hypothesis is largely correlative. Transgenic plants engineered to accumulate proline, mannitol, fructans, trehalose, glycine betaine or ononitol exhibit marginal improvements in salt and/or drought tolerance. While these studies do not dismiss causative relationships between osmolyte levels and stress tolerance, the absolute osmolyte concentrations in these plants are unlikely to mediate osmotic adjustment. Metabolic benefits of osmolyte accumulation may augment the classically accepted roles of these compounds. In re-assessing the functional significance of compatible solute accumulation, it is suggested that proline and glycine betaine synthesis may buffer cellular redox potential. Disturbances in hexose sensing in transgenic plants engineered to produce trehalose, fructans or mannitol may be an important contributory factor to the stress-tolerant phenotypes observed. Associated effects on photoassimilate allocation between root and shoot tissues may also be involved. Whether or not osmolyte transport between subcellular compartments or different organs represents a bottleneck that limits stress tolerance at the whole-plant level is presently unclear. None the less, if osmolyte metabolism impinges on hexose or redox signalling, then it may be important in long-range signal transmission throughout the plant.

https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-3040.1998.00309.x

Dissecting the roles of osmolyte accumulation during stress

Guanylyl cyclases are a family of enzymes that catalyze the conversion of GTP to cGMP. The family comprises both membrane-bound and soluble isoforms that are expressed in nearly all cell types. They are regulated by diverse extracellular agonists that include peptide hormones, bacterial toxins, and free radicals, as well as intracellular molecules, such as calcium and adenine nucleotides. Stimulation of guanylyl cyclases and the resultant accumulation of cGMP regulates complex signaling cascades through immediate downstream effectors, including cGMP-dependent protein kinases, cGMP-regulated phosphodiesterases, and cyclic nucleotide-gated ion channels. Guanylyl cyclases and cGMP-mediated signaling cascades play a central role in the regulation of diverse (patho)physiological processes, including vascular smooth muscle motility, intestinal fluid and electrolyte homeostasis, and retinal phototransduction. Topics addressed in this review include the structure and chromosomal localization of the genes for guanylyl cyclases, structure and function of the members of the guanylyl cyclase family, molecular mechanisms regulating enzymatic activity, and molecular sequences coupling ligand binding to catalytic activity. A brief overview is presented of the downstream events controlled by guanylyl cyclases, including the effectors that are regulated by cGMP and the role that guanylyl cyclases play in cell physiology and pathophysiology.

Guanylyl Cyclases and Signaling by Cyclic GMP

Light- and Guanosine 5′-3-O-(Thio)triphosphate-sensitive Localization of a G Protein and Its Effector on Detergent-resistant Membrane Rafts in Rod Photoreceptor Outer Segments

Light-mediated breakdown of phosphatidylinositol-4,5-bisphosphate in isolated rod outer segments of frog photoreceptor.

Activation of Retinal Guanylyl Cyclase-1 by Ca2+-binding Proteins Involves Its Dimerization

Novel Light-Dark Change of Proline Levels in Halophyte (Mesembryanthemum crystallinum L. ) and Glycophytes (Hordeum vulgare L. and Triticum aestivum L. ) Leaves and Roots under Salt Stress

Fumio Hayashi

Papers

Light- and Guanosine 5′-3-O-(Thio)triphosphate-sensitive Localization of a G Protein and Its Effector on Detergent-resistant Membrane Rafts in Rod Photoreceptor Outer Segments

Light-mediated breakdown of phosphatidylinositol-4,5-bisphosphate in isolated rod outer segments of frog photoreceptor.

Activation of Retinal Guanylyl Cyclase-1 by Ca2+-binding Proteins Involves Its Dimerization

Novel Light-Dark Change of Proline Levels in Halophyte (Mesembryanthemum crystallinum L. ) and Glycophytes (Hordeum vulgare L. and Triticum aestivum L. ) Leaves and Roots under Salt Stress

Roles of Two ATPase-Motif-containing Domains in Cyanobacterial Circadian Clock Protein KaiC