Sulfur Dioxide Enhances Endogenous Hydrogen Sulfide Accumulation and Alleviates Oxidative Stress Induced by Aluminum Stress in Germinating Wheat Seeds

Overview

Journal Oxid Med Cell Longev

Publisher Wiley

Specialties Cell Biology
Endocrinology

Date 2015 Jun 17

PMID 26078810

Citations 8

Authors

Dong-Bo Zhu

Kang-Di Hu

Xi-Kai Guo

Yong Liu

Lan-Ying Hu

Yan-Hong Li

Song-Hua Wang

Hua Zhang

Affiliations

Soon will be listed here.

Abstract

Aluminum ions are especially toxic to plants in acidic soils. Here we present evidences that SO2 protects germinating wheat grains against aluminum stress. SO2 donor (NaHSO3/Na2SO3) pretreatment at 1.2 mM reduced the accumulation of superoxide anion, hydrogen peroxide, and malondialdehyde, enhanced the activities of guaiacol peroxidase, catalase, and ascorbate peroxidase, and decreased the activity of lipoxygenase in germinating wheat grains exposed to Al stress. We also observed higher accumulation of hydrogen sulfide (H2S) in SO2-pretreated grain, suggesting the tight relation between sulfite and sulfide. Wheat grains geminated in water for 36 h were pretreated with or without 1 mM SO2 donor for 12 h prior to exposure to Al stress for 48 h and the ameliorating effects of SO2 on wheat radicles were studied. SO2 donor pretreatment reduced the content of reactive oxygen species, protected membrane integrity, and reduced Al accumulation in wheat radicles. Gene expression analysis showed that SO2 donor pretreatment decreased the expression of Al-responsive genes TaWali1, TaWali2, TaWali3, TaWali5, TaWali6, and TaALMT1 in radicles exposed to Al stress. These results suggested that SO2 could increase endogenous H2S accumulation and the antioxidant capability and decrease endogenous Al content in wheat grains to alleviate Al stress.

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References

Hu L, Hu S, Wu J, Li Y, Zheng J, Wei Z . Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. J Agric Food Chem. 2012; 60(35):8684-93. DOI: 10.1021/jf300728h. View

Yarmolinsky D, Brychkova G, Kurmanbayeva A, Bekturova A, Ventura Y, Khozin-Goldberg I . Impairment in Sulfite Reductase Leads to Early Leaf Senescence in Tomato Plants. Plant Physiol. 2014; 165(4):1505-1520. PMC: 4119034. DOI: 10.1104/pp.114.241356. View

Wang Z, Xu X, Gong Q, Xie C, Fan W, Yang J . Root proteome of rice studied by iTRAQ provides integrated insight into aluminum stress tolerance mechanisms in plants. J Proteomics. 2014; 98:189-205. DOI: 10.1016/j.jprot.2013.12.023. View

Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P . Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell. 2004; 16(10):2693-704. PMC: 520965. DOI: 10.1105/tpc.104.023960. View

Stipanuk M, Dominy Jr J, Lee J, Coloso R . Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J Nutr. 2006; 136(6 Suppl):1652S-1659S. DOI: 10.1093/jn/136.6.1652S. View

Wang Y, Yang Z . Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol. 2005; 46(12):1915-23. DOI: 10.1093/pcp/pci202. View

Ligaba A, Dreyer I, Margaryan A, Schneider D, Kochian L, Pineros M . Functional, structural and phylogenetic analysis of domains underlying the Al sensitivity of the aluminum-activated malate/anion transporter, TaALMT1. Plant J. 2013; 76(5):766-80. DOI: 10.1111/tpj.12332. View

Sharma P, Dubey R . Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep. 2007; 26(11):2027-38. DOI: 10.1007/s00299-007-0416-6. View

Zhang H, Tan Z, Hu L, Wang S, Luo J, Jones R . Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol. 2010; 52(6):556-67. DOI: 10.1111/j.1744-7909.2010.00946.x. View

10.

Li S, Hu K, Hu L, Li Y, Jiang A, Xiao F . Hydrogen sulfide alleviates postharvest senescence of broccoli by modulating antioxidant defense and senescence-related gene expression. J Agric Food Chem. 2014; 62(5):1119-29. DOI: 10.1021/jf4047122. View

11.

Laisk A, Pfanz H, Heber U . Sulfur-dioxide fluxes into different cellular compartments of leaves photosynthesizing in a polluted atmosphere : II. Consequences of SO2 uptake as revealed by computer analysis. Planta. 2013; 173(2):241-52. DOI: 10.1007/BF00403016. View

12.

Zhang S, Du J, Jin H, Li W, Liang Y, Geng B . Endogenous sulfur dioxide aggravates myocardial injury in isolated rat heart with ischemia and reperfusion. Transplantation. 2009; 87(4):517-24. DOI: 10.1097/TP.0b013e318195fe82. View

13.

Surrey K . Spectrophotometric Method for Determination of Lipoxidase Activity. Plant Physiol. 1964; 39(1):65-70. PMC: 550028. DOI: 10.1104/pp.39.1.65. View

14.

LeBel C, Ischiropoulos H, Bondy S . Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol. 1992; 5(2):227-31. DOI: 10.1021/tx00026a012. View

15.

Ding Z, Yan J, Xu X, Li G, Zheng S . WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J. 2013; 76(5):825-35. DOI: 10.1111/tpj.12337. View

16.

Huang W, Yang X, Yao S, LwinOo T, He H, Wang A . Reactive oxygen species burst induced by aluminum stress triggers mitochondria-dependent programmed cell death in peanut root tip cells. Plant Physiol Biochem. 2014; 82:76-84. DOI: 10.1016/j.plaphy.2014.03.037. View

17.

Snowden K, Gardner R . Five genes induced by aluminum in wheat (Triticum aestivum L.) roots. Plant Physiol. 1993; 103(3):855-61. PMC: 159056. DOI: 10.1104/pp.103.3.855. View

18.

Giraud E, Ivanova A, Gordon C, Whelan J, Considine M . Sulphur dioxide evokes a large scale reprogramming of the grape berry transcriptome associated with oxidative signalling and biotic defence responses. Plant Cell Environ. 2011; 35(2):405-17. DOI: 10.1111/j.1365-3040.2011.02379.x. View

19.

Jin H, DU S, Zhao X, Wei H, Wang Y, Liang Y . Effects of endogenous sulfur dioxide on monocrotaline-induced pulmonary hypertension in rats. Acta Pharmacol Sin. 2008; 29(10):1157-66. DOI: 10.1111/j.1745-7254.2008.00864.x. View

20.

Noji M, Saito M, Nakamura M, Aono M, Saji H, Saito K . Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol. 2001; 126(3):973-80. PMC: 116454. DOI: 10.1104/pp.126.3.973. View