Hydrogen sulfide and plant adaptation to abiotic stressors

Hydrogen sulfide (H₂S) is one of the key gasotransmitters in plant and animal cells. The term “hydrogen sulfide” means not only H₂S as a dissolved gaseous compound, but also the HS- anion, into which, under physiologically normal conditions, about 80% of molecular hydrogen sulfide is converted. One of the most notable hydrogen sulfide physiological effects is the activation of adaptive plant responses. However, the activation mechanisms of plant stress-protective systems under the H₂S influence, direct targets of its action, signaling and hormonal mediators providing physiological effects, remain poorly understood. Analysis and systematization of information on hydrogen sulfide synthesis, signaling, and activation of adaptive reactions with its participation became the aim of this review. Hydrogen sulfide synthesis. To date, it has been found that in plants hydrogen sulfide can be synthesized using six enzymes (See Fig. 1). Conversion of L-cysteine to pyruvate catalyzed by L-cysteine desulfhydrase with release of hydrogen sulfide and ammonium is considered as one of the main ways of synthesizing H₂S in plants. It is also possible to form hydrogen sulfide from D-cysteine under the action of D-cysteine desulfhydrase. Hydrogen sulfide can also be synthesized by sulfite reduction with the participation of sulfite reductase. Formation of hydrogen sulfide in plants involving β-cyanoalanine synthase, cysteine synthase and carbonic anhydrase is also expected. Hydrogen sulfide signaling. Hydrogen sulfide does not have specific molecular receptors. It is assumed that primary molecular effects of H₂S are associated with S-sulfhydration (persulfidation) - conversion of -SH cysteine residues to -SSH. The most common proteins whose state is regulated by sulfhydration are peroxyredoxins, which, in turn, are among the key participants in cellular redox regulation. Hydrogen sulfide is also involved in processes of redox regulation occuring with participation of reactive oxygen species (ROS) and nitric oxide (NO), and can affect cell calcium homeostasis (See Fig. 2). In this case, however, the sequence of arrangement of these intermediaries in formation of various adaptive reactions of plants in many cases remains unknown. There is evidence of an increase in the ROS content in plant cells under the influence of hydrogen sulfide, due, primarily, to the activation of NADPH oxidase. At the same time, synthesis of hydrogen sulfide can be induced by an action of hydrogen peroxide on plant objects. Hydrogen sulfide can directly and indirectly influence activity and expression of antioxidant enzyme genes, which also affects cell redox homeostasis. It was shown that hydrogen sulfide and nitric oxide can act on the same protein targets, causing effects of persulfidation or nitrosylation. Moreover, NO and H₂S also affect the intracellular content of each other. Hydrogen sulfide is in a rather complex functional interaction with calcium ions. Activation of hydrogen sulfide synthesis associated with increased expression of L-cysteine desulfhydrase gene can be induced with calcium and calmodulin. On the other hand, hydrogen sulfide can cause an opening of calcium channels of plant cells. Hydrogen sulfide interacts with a complex network of hormonal signaling too (See Fig. 2). In particular, its synthesis can be induced by abscisic acid (ABA). On the other hand, H₂S can mediate physiological effects of ABA. Hydrogen sulfide can activate synthesis of jasmonic acid in plants. Also, H₂S is involved in plant adaptive reactions induction under influence of salicylic acid and polyamines. In general, hydrogen sulfide is involved in a complex regulatory network of signaling and hormonal mediators. Participation in plant adaptation. In response to the impact of many stressors (high and low temperatures, dehydration, salinization), the content of endogenous hydrogen sulfide in plants increases. Moreover, mutants defective in the hydrogen sulfide synthesis were not resistant to action of these stress factors. Plant treatment with hydrogen sulfide donors (in particular, sodium hydrosulfide NaHS) increases resistance of plants to stress temperatures, drought, salt stress, action of heavy metals, UV-B and other factors (See Table). Hydrogen sulfide has a pronounced activating effect on expression of antioxidant enzyme genes, accumulation of polyfunctional low-molecular-weight protective compounds, in particular proline and sugars. Of particular importance for plant adaptation is the accumulation under the influence of hydrogen sulfide of a wide range of secondary metabolites, including phenolic compounds and flavonoids, which have a pronounced antioxidant effect. Hydrogen sulfide is also involved in regulation of plant stomatal reactions. Dependence of the stomata closing process under osmotic and salt stress on the activity of cysteine desulfhydrase and H₂S synthesis was shown. The effect of hydrogen sulfide on stomatal aperture, as well as other stomata closing inducers, is associated with a change in the ion channels state, in particular, potassium channels (K⁺_out) of guard cells. ROS, calcium ions and, possibly, components of lipid signaling are involved in the implementation of these effects of hydrogen sulfide. Hydrogen sulfide donors can be used not only to induce adaptive reactions of plants, but also in storage technology for agricultural products. The use of NaHS during storage of fruit and berries prevents their ripening and aging, contributes to the preservation of a pool of antioxidants, in particular, ascorbic acid, phenolic compounds and flavonoids. Also, hydrogen sulfide can be used to extend the life of cut flowers. A further study of stress-protective effects of hydrogen sulfide will allow, on the one hand, to more deeply understand the adaptation mechanisms, and, on the other hand, to create theoretical foundations for new approaches in agrobiotechnology. The paper contains 2 Figures, 1 Table and 93 References.

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