Abstract
Drought is an environmental factor that deeply impacts wheat yield and quality. Hydrogen sulfide (H2S) is a known regulator of drought resistance in plants. To preliminarily elucidate the regulatory mechanisms of H2S on drought tolerance, the effects of H2S on drought-responsive genes were investigated by transcriptome analysis. As a result, a total of 7552 transcripts not only responded to drought stress but also exhibited differential expression relative to the polyethylene glycol (PEG) treatment (P) and the NaHS pretreatment with PEG treatment (SP). GO categories of ‘transport’ were especially enriched under the SP treatment and ion transport categories (especially ‘iron ion transport’) were more significantly enriched among up-regulated transcripts in SP versus P treatments (SP.vs.P). Indeed, a higher translocation of iron from root to shoot and iron availability in shoots was detected in SP compared to P. The KEGG pathway of ‘ribosome biogenesis in eukaryotes’, ‘protein processing in endoplasmic reticulum’, ‘fatty acid degradation’, and ‘cyanoamino acid metabolism’ was induced by H2S under drought stress. Further, H2S was involved in plant hormones signal transduction, and drought-induced transcription factors, protein kinases, and functional genes exhibited higher expression levels under SP relative to P. Additionally, several effectors or master regulatory genes of H2S were identified genome-wide. Summarily, these results showed that H2S alleviated drought damage probably related to transport systems, plant hormones signal transduction, protein processing pathway, fatty acids and amino acids metabolism, which provides a guide for future experimentation to analyze hydrogen sulfide-dependent drought tolerance mechanisms in wheat.
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References
Aimar D, Calafat M, Andrade AM, Carassay L, Abdala GI, Molas ML (2011) Drought tolerance and stress hormones: from model organisms to forage crops. Plants Environ, pp 137–164
Akdogan G, Tufekci ED, Uranbey S, Unver T (2016) miRNA-based drought regulation in wheat. Funct Integr Genom 16:221–233
Al-Karaki GN, Al-Raddad A (1997) Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Mycorrhiza 7:83–88
Baloglu MC, Inal B, Kavas M, Unver T (2014) Diverse expression pattern of wheat transcription factors against abiotic stresses in wheat species. Gene 550:117–122
Bezrukova MV, Sakhabutdinova R, Fathutdinova RA, Kyldiarova I, Shakirova F (2001) The role of hormonal changes in protective action of salicylic acid on growth of wheat seedlings under water deficit. Agrochemiya (Russ) 2:51–54
Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MSA (2014) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut R 21:717–731
Budak H, Kantar M, Yucebilgili Kurtoglu K (2013) Drought tolerance in modern and wild wheat. Sci World J 2013:548246
Cao M, Liu X, Zhang Y, Xue X, Zhou XE, Melcher K, Gao P, Wang F, Zeng L, Zhao Y, Zhao Y, Deng P, Zhong D, Zhu JK, Xu HE, Xu Y (2013) An ABA-mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Res 23:1043–1054
Cassin G, Mari S, Curie C, Briat J-F, Czernic P (2009) Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine. J Exp Bot 60(4):1249–1259
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought from genes to the whole plants. Funct Plant Biol 30:239–264
Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He XJ, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493
Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He XJ, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318
Chen J, Wu FH, Shang YT, Wang WH, Hu WJ, Simon M, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency. J Exp Bot 66:6605–6622
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236
Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966
Dawood M, Cao F, Jahangir MM, Zhang GP, Wu FB (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209:121–128
De-Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306
Du H, Wu N, Fu J, Wang S, Li X, Xiao J, Xiong L (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J Exp Bot 63:6467–6480
Duan BB, Ma YH, Jiang MG, Yang F, Ni L, Lu W (2015) Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul 75:33–44
Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genom 9:377–396
Fang H, Jing T, Liu Z, Zhang L, Jin Z, Pei Y (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481
Fariduddin Q, Khanam S, Hasan SA, Ali B, Hayat S, Ahmad A (2009) Effect of 28-homobrassinolide on the drought stress-induced changes in photosynthesis and antioxidant system of Brassica juncea L. Acta Physiol Plant 31:889–897
Farooq M, Wahid A, Basra SMA, Islam-ud-Din (2009) Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J Agron Crop Sci 195(4):262–269
García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984
Graziano M, Lamattina L (2007) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–960
Hou Z, Liu J, Hou L, Li X, Liu X (2011) H2S may function downstream of H2O2 in jasmonic acid-induced stomatal closure in Vicia faba. Chin Bull Bot 46:396–406
Hou Z, Wang L, Liu J, Hou L, Liu X (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol 55:277–289
Hu LY, Hu SL, Wu J, Li HY, Zheng JL, Wei ZJ, Liu J, Wang LH, Liu YS, Zhang H (2012) Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. J Agric Food Chem 60:8684–8693
Im-Kim J, Baek D, Park HC, Chun HJ, Oh DH, Lee MK, Cha JY, Kim WY, Kim MC, Chung WS, Bohnert HJ, Lee SY, Bressan RA, Lee SW, Yun DJ (2013) Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol Plant 6:337–349
Jin ZP, Shen JP, Qiao ZJ, Yang GD, Wang R, Pei YX (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486
Jin ZP, Xue SW, Luo YN, Tian BH, Fang HH, Li H, Pei YX (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46
Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364
Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229
Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297
Lee M, Jung JH, Han DY, Seo PJ, Park WJ, Park CM (2012) Activation of a flavin monooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis. Planta 235:923–938
Li J, Sima W, Ouyang B, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y, Feng Y, Hao Y, Ye Z (2012a) Tomato SlDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. J Exp Bot 63:6407–6420
Li L, Wang Y, Shen W (2012b) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631
Li ZG, Gong M, Liu P (2012c) Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas. Acta Physiol Plant 34:2207–2213
Li ZG, Gong M, Xie H, Yang L, Li J (2012d) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185–186:185–189
Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572
Li H, Gao MQ, Xue RL, Wang D, Zhao HJ (2015a) Effect of hydrogen sulfide on D1 protein in wheat under drought stress. Acta Physiol Plant 37:225
Li ZG, Long WB, Yang SZ, Wang YC, Tang JH, Wen L, Zhu BY, Min X (2015b) Endogenous hydrogen sulfide regulated by calcium is involved in thermotolerance in tobacco Nicotiana tabacum L. suspension cell cultures. Acta Physiol Plant 37:1–11
Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012) Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation. J Plant Growth Regul 31:519–528
Ma X, Zhu X, Li C, Song Y, Zhang W, Xia G, Wang M (2015) Overexpression of wheat NF-YA10 gene regulates the salinity stress response in Arabidopsis thaliana. Plant Physiol Biochem 86:34–43
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158
Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793
Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327
Moumeni A, Satoh K, Kondoh H, Asano T, Hosaka A, Venuprasad R, Serraj R, Kumar A, Leung H, Kikuchi S (2011) Comparative analysis of root transcriptome profiles of two pairs of drought-tolerant and susceptible rice near-isogenic lines under different drought stress. BMC Plant Biol 11:1
Msilini N, Zaghdoudi M, Govindachary S, Lachaâl M, Ouerghi Z, Carpentier R (2011) Inhibition of photosynthetic oxygen evolution and electron transfer from the quinone acceptor QA− to QB by iron deficiency. Photosynth Res 107:247–256
Msilini N, Essemine J, Zaghdoudi M, Harnois J, Lachaâl M, Ouerghi Z, Carpentier R (2013) How does iron deficiency disrupt the electron flow in photosystem I of lettuce leaves? J Plant Physiol 170:1400–1406
Nir I, Moshelion M, Weiss D (2014) The Arabidopsis GIBBERELLIN METHYL TRANSFERASE 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant Cell Environ 37:113–123
Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Phan Tran LS (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183
Okay S, Derelli E, Unver T (2014) Transcriptome-wide identification of bread wheat WRKY transcription factors in response to drought stress. Mol Genet Genom 289:765–781
Olson KR (2009) Is hydrogen sulfide a circulating ‘gasotransmitter’ in vertebrate blood? Biochim Biophys Acta 1787:856–863
Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol J 9:747–758
Polle A, Klein T, Kettner C (2013) Impact of cadmium on young plants of Populus euphratica and P. × canescens, two poplar species that differ in stress tolerance. New Forest 44:13–22
Remy E, Cabrito TR, Baster P, Batista RA, Teixeira MC, Friml J, Sá-Correia I, Duque P (2013) A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis. Plant Cell 25:901–926
Sang Y, Zheng S, Li W, Huang B, Wang X (2001) Regulation of plant water loss by manipulating the expression of phospholipase Dα. Plant J 28:135–144
Saruhan N, Saglam A, Kadioglu A (2012) Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol Plant 34:97–106
Scuffi D, Álvarez C, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076
Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139
Shan C, Dai H, Sun Y (2012) Hydrogen sulfide protects wheat seedlings against copper stress by regulating the ascorbate and glutathione metabolism in leaves. Aust J Crop Sci 6:248–254
Sharma S (2007) Adaptation of photosynthesis under iron deficiency in maize. J Plant Physiol 164:1261–1267
Shen J, Xing T, Yuan H, Liu Z, Jin Z, Zhang L, Pei Y (2013) Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS One 8:e77047
Shi H, Chen L, Ye T, Liu X, Ding K, Chan Z (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Biochem 82:209–217
Shi H, Ye T, Han N, Bian H, Liu X, Chan Z (2015) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Integr Plant Biol 57:628–640
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Shu L, Lou Q, Ma C, Ding W, Zhou J, Wu J, Feng F, Lu X, Luo L, Xu G, Mei H (2011) Genetic, proteomic and metabolic analysis of the regulation of energy storage in rice seedlings in response to drought. Proteomics 11:4122–4138
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141
Sun J, Wang R, Zhang X, Yu YC, Zhao R, Li ZY, Chen SL (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74
Tan BH, Wong PTH, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3–10
Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S, Jensen P (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci USA 100:16119–16124
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van-Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515
Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138
Wang SS, Liu ZZ, Sun C, Shi QH, Yao YX, You CX, Hao YJ (2012a) Functional characterization of the apple MhGAI1 gene through ectopic expression and grafting experiments in tomatoes. J Plant Physiol 169:303–310
Wang Y, Li L, Cui W, Xu S, Shen WB, Wang R (2012b) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119
Wang LX, Hou ZH, Hou LX, Zhao FG, Liu X (2013) H2S induced by H2O2 mediates drought-induced stomatal closure in Arabidopsis thaliana. Chin Bull Bot 47:217–225 In Chinese
Xie YJ, Zhang C, Lai DW, Sun Y, Samma MK, Zhang J, Shen WB (2014) Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J Plant Physiol 171:53–62
Xoconostle-Cázares B, Ramirez-Ortega FA, Flores-Elenes L, Ruiz-Medrano R (2010) Drought tolerance in crop plants. Am J Plant Physiol 5:241–256
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:1
Zawaski C, Busov VB (2014) Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. PLoS One 9:e86217
Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529
Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094
Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250
Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009c) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889–1901
Zhang H, Dou W, Jiang CX, Wei ZJ, Liu J, Jones RL (2010a) Hydrogen sulfide stimulates β-amylase activity during early stages of wheat grain germination. Plant Signal Behav 5:1031–1033
Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010b) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32:849–857
Zhang H, Hu SL, Zhang ZJ, Hu LY, Jiang CX, Wei ZJ, Liu J, Wang LH, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257
Zhang Q, Li J, Zhang W, Yan S, Wang R, Zhao J, Li Y, Qi Z, Sun Z, Zhu Z (2012) The putative auxin efflux carrier OsPIN3t is involved in the drought stress response and drought tolerance. Plant J 72:805–816
Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247
Acknowledgements
This research was supported by the National Natural Science Foundation of China (31501238), the fund of the State Key Laboratory of Wheat and Maize Crop Science (SKL2014KF-06), Scientific Research Foundation of the Higher Education Institutions of He’nan Province, China (15A180040), and Science and Technology Innovation Fund of Henan Agricultural University (KJCX2015A13).
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HL participated in the experimental design and performed most of the experiments and data analysis, and drafted the manuscript. ML and XLW performed the plant preparation, sample collection, and RNA extraction. XZ and RLX carried out the qRT-PCR experiments. HJZ and YDZ helped to draft and revise the manuscript. All authors read and approved the final manuscript.
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Li, H., Li, M., Wei, X. et al. Transcriptome analysis of drought-responsive genes regulated by hydrogen sulfide in wheat (Triticum aestivum L.) leaves. Mol Genet Genomics 292, 1091–1110 (2017). https://doi.org/10.1007/s00438-017-1330-4
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DOI: https://doi.org/10.1007/s00438-017-1330-4