научная статья по теме HYDROGEN SULFIDE: A MULTIFUNCTIONAL GASEOUS MOLECULE IN PLANTS Биология

Текст научной статьи на тему «HYDROGEN SULFIDE: A MULTIFUNCTIONAL GASEOUS MOLECULE IN PLANTS»

ФИЗИОЛОГИЯ РАСТЕНИЙ, 2013, том 60, № 6, с. 776-783

= ОБЗОРЫ =

УДК 581.1

HYDROGEN SULFIDE: A MULTIFUNCTIONAL GASEOUS MOLECULE

IN PLANTS1

© 2013 Z. G. Li

School of Life Sciences, Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province,

Yunnan Normal University, Kunming, P.R. China Received October 12, 2012

Hydrogen sulfide (H2S), a gaseous transmitter, has long been considered as a phytotoxin, but nowadays as a small molecule with multiple functions fulfilled at low concentrations. H2S has many positive effects on plant growth, development, and the acquisition of plant stress tolerance. The focus of this review is to summarize the generation and properties of hydrogen sulfide and its potential physiological functions, including mediating stomatal movements; mediating the responses to abiotic stressors, such as heavy metals, salt, drought and heating; involving in organogenesis and growth; regulating senescence; priming seed germination; and enhancing photosynthesis. Future prospects are also presented.

Keywords:plants - abiotic stress - hydrogen sulfide - signaling molecule - stress tolerance

DOI: 10.7868/S0015330313060055

INTRODUCTION

Hydrogen sulfide (H2S), colorless and flammable gas, has long been considered as a phytotoxin, which is harmful to plant growth and development, but nowadays as a small molecule with multiple functions fulfilled in plants at low concentrations [1]. In many plant species, such as alfalfa, grape, or lettuce, fumigation with H2S caused lesions on leaves, defoliation, and reduced plant growth [1]. It was also found repeatedly that H2S inhibited oxygen release from young

1 This text was submitted by the author in English.

Abbreviations'. AOA - aminooxyacetic acid; APR - adenosine-5-phosphosulphate reductase; APX - ascorbate peroxidase; CaM -calmodulin; CAT - catalase; CPZ - chlorpromazine; DPI -diphenylene iodonium; GYY4137 - p-(methoxyphenyl)morpholi-no-phosphine-dithionic acid; HM - heavy metals; HO-1/CO -haem oxygenase-1/carbon monoxide; L-/D-CD - L-/D-cys-teine desulfhydrase; LSCM - laser scanning confocal microscopy; MS - 3-mercaptopyruvate sulfurtransferase; NOX - NADPH oxidase; OAS-TL - O-acetyl-L-serine (thiol) lyase; P5CS - A1-pyrroline-5-carboxylate synthetase; PME - pectin methyl-esterase; POD - guaiacol peroxidase; ppb - parts per billion; ProDH - proline dehydrogenase; RWC - relative water content; SHAM - salicylhydroxamic acid; SNP - sodium nitroprusside; SOD - superoxide dismutase; TFP - triuoperazine; RBCL -Rubisco large subunit; RBCS - Rubisco small subunit; RR - ruthenium red; Rubisco - ribulose-1,5-bisphosphate carboxylase. Corresponding author. Li Zhong-Guang. School of Life Sciences, Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092 P.R. China. Fax. +86-871-594-1365; e-mail. zhongguang_li@163.com

seedlings of six rice cultivars and suppressed the uptake of nutrients, such as phosphorus [1, 2]; these results support the role of H2S as a phytotoxin. In contrast, the lower levels of fumigation, 100 parts per billion (ppb), caused a substantial increase in the growth of alfalfa, lettuce, and sugar beet; it was also noted that in some rice cultivars H2S could promote nutrient uptake [1].

Increasing evidence illustrates that H2S acts as an important signaling molecule to regulate many physiological processes in animal systems [1]. In plant systems, a lot of physiological functions of H2S have been found. Lisjak et al. [3] reported that H2S caused stomatal opening in the light and prevented stomatal closure in the dark by reducing the accumulation of NO in Arabidopsis thaliana, while drought stress led to sto-matal closure through the increase in the content of H2S due to the enhanced expression and activity of D-/L-cysteine desulfhydrase (L-/D-CD), a key enzyme of H2S biosynthesis in leaves of Vicia faba [4]. Our previous results also found that H2S was a mediator in H2O2-induced seed germination of Jatropha curcas [5], and NaHS pretreatment significantly increased a survival percentage of maize seedlings and tobacco suspension cultured cells under heat stress and regrowth ability after heat stress by alleviating a decrease in the vitality of cells and accumulation of MDA [6, 7].

For excellent additional knowledge, I refer readers to wonderful review written more recently [1]. The fo-

Fig. 1. Hydrogen sulfide biosynthesis in plants.

L-cysteine desulfhydrase (L-CD; EC 4.4.1.1) or D-cysteine desulfhydrase (D-CD; EC 4.4.1.15) specifically metabolizes L-cys-teine or D-cysteine to produce H2S, pyruvate, and ammonium or sulfite is reduced by sulfite reductase (SIR; EC 1.8.7.1) to H2S in plants (adapted from Wang [1]).

cus of this review is to summarize current knowledge about H2S generation and properties and its potential physiological functions, including mediating stomatal closure; mediating the responses to abiotic stressors, such as heavy metals, salt, drought, and heating; involving in organogenesis and growth; regulating senescence; priming seed germination; and enhancing photosynthesis. Future prospects are also presented.

lated to H2S production in plants [1]. L-CD specifically metabolizes L-cysteine to produce H2S, pyruvate, and ammonium [1]. L-CD activity and expression can be up-regulated when plants are attacked by pathogen, and this enzyme could be a key factor in releasing H2S during a plant defense response [1]. Additionally, in producing H2S, D-CD (EC 4.4.1.15) only decomposes D-cysteine, not L-cysteine (fig. 1).

THE GENERATION OF HYDROGEN SULFIDE

A number of studies have shown that many plant species can generate H2S, suggesting that it may be an endogenous chemical, suitable to act as a signaling molecule [1]. Wilson et al. [8] found, using a sulfur-specific flame photometric detector, that cucumber, squash, pumpkin, soybean, and cotton, amongst other plants, were able to generate H2S. Additionally, the rate of H2S emission was substantially increased when leaves were fed with sulfate through their petioles or when the plant roots were mechanically damaged [2]. Using cucumber as a model species, Sekiya et al. [9] also illustrated that young leaves emitted much more H2S than mature leaves. Furthermore, Rennenberg [2] found that pumpkin leaves emitted H2S if supplied with sulfate, sulfite, cysteine, or SO2, but different metabolic routes were used for different sulfur sources.

Further results illustrated that cysteine-synthesiz-ing and degrading enzymes, such as O-acetyl-L-serine (thiol) lyase (OAS-TL; EC 4.2.99.8), L-cysteine desulfhydrase (L-CD; EC 4.4.1.1), and 3-mercaptopyru-vate sulfurtransferase (MS; EC 2.8.1.2) are closely re-

THE PROPERTIES OF HYDROGEN SULFIDE

As mentioned above, H2S is a colorless and flammable gas. Its smell is characteristic of rotten eggs or the obnoxious odor of a blocked sewer. H2S is the sulfur analog of water molecule and can be oxidized in a series of reactions to form sulfur dioxide (SO2), sulfates, such as sulfuric acid, and elemental sulfur [1]. It has a molecular weight of 34.08 and a vapor density (d) of 1.19, i.e., it is heavier than air (d = 1.0). Its boiling point is -60.3°C, melting point is -82.3°C, and freezing point is -86°C [3].

Temperature also affects the solubility of H2S: at room temperature (20°C), one gram of H2S will dissolve in 242 mL of H2O, 94.3 mL of absolute ethanol, or 48.5 mL of diethyl ether. H2S is a highly lipophilic molecule, which easily penetrates lipid bilayer of cell membranes. H2S also evaporates relatively easy from aqueous solutions (vapor pressure = 18.75 x 10-5 Pa) [1]. It is a weak acid in aqueous solution with an acid dissociation constant (pKJ of 6.76 at 37°C. It can dissociate into H+ and hydrosulfide anion (HS), which in

ABA

L-/D-CD

Stomatal closure -H2O2

NOX

L-/D-CD

H2S

• Stomatal opening

Ca-

2+.

Fig. 2. Schematic diagram of H2S-regulated stomatal movements in plants.

H2S controls stomatal movements via cross-talk with second messengers, such as ABA, Eth, NO, H2O2, Ca2+. Arrows indicate positive effects, blunt line (-) indicates negative effect, question mark (?) indicates that the interaction between H2S and Ca2+ is not confirmed. ABA - abscisic acid; Eth - ethylene; L-/D-CD - L-/D-cysteine desulfhydrase; NOX - NADPH oxidase.

turn may dissociate into H+ and sulfide anion (S2 ) in the following reaction. H2S ^ H+ + HS- ^ 2 H+ + S2- [1].

PHYSIOLOGICAL FUNCTIONS OF HYDROGEN SULFIDE

Mediator of stomatal movements

The loss of water from a plant occurs mainly through leaf stomata; stomatal movements involve many second messengers, such as Ca2+, H2O2, NO, ABA, and H2S cross-talking with each other; it is a key factor affecting transpiration in plants (fig. 2). Lisjak et al. [3] investigated the effects of NaSH and GYY4137 on stomatal closure in A. thaliana and found that NaSH and GYY4137 reduced the accumulation of NO in guard cells, which in turn caused stomatal opening in the light and prevented stomatal closure in the dark. Similarly, both NaSH and GYY4137 reduced the accumulation of NO induced by ABA treatment of leaf tissues in A. thaliana [10]. These results suggest a mode of action for H2S in plant cell signaling pathways. Additionally, the H2S scavenger hypotaurine and H2S synthesis inhibitors (aminooxyacetic acid (AOA), hydroxylamine, potassium pyruvate, and ammonia) inhibited drought-induced stomatal closure [1]. Moreover, drought stress enhanced the level of hydrogen peroxide (H2O2) in guard cells and increased the expression and activity ofD-/L-CD as well as the content of H2S in leaves but had no significant effect in mutants atrbohD, atrbohF, and atrbohD/F [1]. In contrast, the H2O2 scavenger ascorbic acid and

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