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Transcriptome profiling and identification of functional genes involved in H2S response in grapevine tissue cultured plantlets

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Abstract

Hydrogen sulfide (H2S), a small bioactive gas, has been proved functioning in plant growth and development as well as alleviation of abiotic stresses, which including promoting seed germination, accelerating embryonic root growth, regulating flower senescence, inducing stomatal closure, and defending drought, heat, heavy metals and osmotic stresses etc. However, the molecular functioning mechanism of H2S was still unclear. The primary objective of this research was to analyze the transcriptional differences and functional genes involved in the H2S responses. In details, 4-week-old plantlets in tissue culture of grapevine (Vitis vinifera L.) cultivar ‘Zuoyouhong’ were sprayed with 0.1 mM NaHS for 12 h, and then transcriptome sequencing and qRT-PCR analysis were used to study the transcriptional differences and functional genes involved in the H2S responses. Our results indicated that 650 genes were differentially expressed after H2S treatment, in which 224 genes were up-regulated and 426 genes were down-regulated. The GO enrichment analysis and KEGG enrichment analysis results indicated that the up-regulated genes after H2S treatment focused on carbon metabolism, biosynthesis of amino acids, and glycolysis/gluconeogenesis, and the down-regulated genes were mainly in metabolic pathways, biosynthesis of secondary metabolites, and plant hormone signal transduction. Analyzing the transcription factor coding genes in details, it was indicated that 10 AP2/EREBPs, 5 NACs, 3 WRKYs, 3 MYBs, and 2 bHLHs etc. transcription factor coding genes were up-regulated, while 4 MYBs, 3 OFPs, 3 bHLHs, 2 AP2/EREBPs, 2 HBs etc. transcription factor coding genes were down-regulated. Taken together, H2S increased the productions in secondary metabolites and a variety of defensive compounds to improve plant development and abiotic resistance, and extend fruits postharvest shelf life by regulating the expression of AP2/EREBPs, WRKYs, MYBs, CABs, GRIP22, FERRITINs, TPSs, UGTs, and GHs etc.

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References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15(1):63–78

    Article  CAS  Google Scholar 

  • Agarwal M, Hao Y, Kapoor A, Dong C, Fujii H, Zheng X, Zhu J (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281(49):37636–37645

    Article  CAS  Google Scholar 

  • Ali B, Gill RA, Yang S, Gill MB, Ali S, Rafiq MT, Zhou W (2014) Hydrogen sulfide alleviates cadmium-induced morpho-physiological and ultrastructural changes in Brassica napus. Ecotoxicol Environ Saf 110:197–207

    Article  CAS  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106

    Article  CAS  Google Scholar 

  • Briat JF, Ravet K, Arnaud N, Duc C, Boucherez J, Touraine B, Cellier F, Gaymard F (2010) New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Bot 105:811–822

    Article  CAS  Google Scholar 

  • Chen J, Wu FH, Shang YT, Wang WH, Hu WJ, Simon M, Liu X, Shangguan ZP, Zheng HL (2015a) Hydrogen sulfide improves adaptation of Zea mays seedlings to iron deficiency. J Exp Bot 66(21):6605–6622

    Article  CAS  Google Scholar 

  • Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015b) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516

    Article  CAS  Google Scholar 

  • Chen J, Shang YT, Wang WH, Chen XY, He EM, Zheng HL, Shangguan Z (2016) Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings. Front Plant Sci 7:1173

    PubMed  PubMed Central  Google Scholar 

  • Chen Z, Chen M, Jiang M (2017) Hydrogen sulfide alleviates mercury toxicity by sequestering it in roots or regulating reactive oxygen species productions in rice seedlings. Plant Physiol Biochem 111:179–192

    Article  CAS  Google Scholar 

  • Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Davies C, Robinson SP (2000) Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. Plant Physiol 122:803–812

    Article  CAS  Google Scholar 

  • Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984

    Article  CAS  Google Scholar 

  • Grubb CD, Zipp BJ, Ludwig-muller J, Masuno MN, Molinski TF, Abel S (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40(6):893–908

    Article  CAS  Google Scholar 

  • Guo C, Guo R, Xu X, Gao M, Li X, Song J, Zheng Y, Wang X (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65:1513–1528

    Article  CAS  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471

    Article  CAS  Google Scholar 

  • Harrington HM, Smith IK (1980) Cysteine metabolism in cultured tobacco cells. Plant Physiol 65:151–155

    Article  CAS  Google Scholar 

  • Hossain MA, Ku ZG, Hoque TS, Burritt DJ, Fujita M, Munne-Bosch S (2018) Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 255(1):399–412

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jansson S (1999) A guide to the identification of the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240

    Article  CAS  Google Scholar 

  • Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46

    Article  CAS  Google Scholar 

  • Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13(1):544

    Article  CAS  Google Scholar 

  • Khan MN, Mobin M, Abbas ZK, Siddiqui MH (2017) Nitric oxide-induced synthesis of hydrogen sulfide alleviates osmotic stress in wheat seedlings through sustaining antioxidant enzymes, osmolyte accumulation and cysteine homeostasis. Nitric Oxide 68:91–102

    Article  CAS  Google Scholar 

  • Kharbech O, Houmani H, Chaoui A, Corpas FJ (2017) Alleviation of Cr(VI)-induced oxidative stress in maize (Zea mays L.) seedlings by NO and H2S donors through differential organ-dependent regulation of ROS and NADPH-recycling metabolisms. J Plant Physiol 219:71–80

    Article  CAS  Google Scholar 

  • Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A mutation of the mitochondrial ABC transporter stat1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100

    Article  CAS  Google Scholar 

  • Lai D, Mao Y, Zhou H, Li F, Wu M, Zhang J, He Z, Cui W, Xie Y (2014) Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa. Plant Sci 225:117–129

    Article  CAS  Google Scholar 

  • Latchman DS (1997) Transcription factors: an overview. Int J Biochem B 29(12):1305–1312

    Article  CAS  Google Scholar 

  • Leon S, Touraine B, Briat JF, Lobreaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a Nifs-like plastidial cysteine desulphurase. Biochem J 366:557–564

    Article  CAS  Google Scholar 

  • Li ZG, Ding XJ, Du PF (2013) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747

    Article  CAS  Google Scholar 

  • Ma Q, Zhang G, Hou L, Wang W, Hao J, Liu X (2015) Vitis vinifera VvWRKY13 is an ethylene biosynthesis-related transcription factor. Plant Cell Rep 34(9):1593–1603

    Article  CAS  Google Scholar 

  • Mancardi D, Penna C, Merlino A, DelSoldato P, Wink DA, Pagliaro P (2009) Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide. Biochim Biophys Acta 1787:864–872

    Article  CAS  Google Scholar 

  • Marchive C, Mzid R, Deluc L, Barrieu F, Pirrello J, Gauthier A, Corio Costet MF, Regad F, Cailleteau B, Hamdi S (2007) Isolation and characterization of a Vitis vinifera transcription factor, VvWRKY1, and its effect on responses to fungal pathogens in transgenic tobacco plants. J Exp Bot 58:1999–2010

    Article  CAS  Google Scholar 

  • Marchive C, Leon C, Kappel C, Coutos-Thevenot P, Corio-Costet MF, Delrot S, Lauvergeat V (2013) Over-expression of VvWRKY1 in grapevines induces expression of jasmonic acid pathway-related genes and confers higher tolerance to the downy mildew. PLoS ONE 8:e54185

    Article  CAS  Google Scholar 

  • Mei Y, Chen H, Shen W, Shen W, Huang L (2017) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17(1):162

    Article  Google Scholar 

  • Merz RP, Moser T, Holl J, Kortekamp A, Buchholz G, Zyprian E, Bogs J (2015) The transcription factor VvWRKY33 is involved in the regulation of grapevine (Vitis vinifera) defense against the oomycete pathogen Plasmopara viticola. Physiol Plant 153:365–380

    Article  CAS  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2011) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96

    Article  Google Scholar 

  • Mostofa MG, Rahman A, Ansary MMU, Watanabe A, Fujita M, Tran LS (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078

    Article  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  Google Scholar 

  • Ni ZJ, Hu KD, Song CB, Ma RH, Li ZR, Zheng JL, Fu LH, Wei ZJ, Zhang H (2016) Hydrogen sulfide alleviates postharvest senescence of grape by modulating the antioxidant defenses. Oxid Med Cell Longev 8:4715651

    Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants—from the field to the test tube and back. Plant Biol 9:582–588

    Article  CAS  Google Scholar 

  • Peng X, Liu H, Wang D, Shen S (2016) Genome-wide identification of the Jatropha curcas MYB family and functional analysis of the abiotic stress responsive gene JcMYB2. BMC Genomics 17:251

    Article  Google Scholar 

  • Priest DM, Ambrose SJ, Vaistij FE, Elias L, Higgins GS, Ross AR, Abrams SR, Bowles D (2006) Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46:492–502

    Article  CAS  Google Scholar 

  • Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57:400–412

    Article  CAS  Google Scholar 

  • Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37(5):1059–1073

    Article  CAS  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  Google Scholar 

  • Schmidt A (1982) A cysteine desulfhydrase from spinach leaves specific for d-cysteine. Z Pflanzenphysiol 107:301–312

    Article  CAS  Google Scholar 

  • Schwartz E, Stasys R, Aebersold R, McGrath JM, Green BR, Pichersky E (1991) Sequence of a tomato gene encoding a third type of LHCII chlorophyll a/b-binding polypeptide. Plant Mol Biol 17:923–925

    Article  CAS  Google Scholar 

  • Scuffi D, Alvarez C, Laspina N, Gotor C, Lamattina L, Garcia-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(4):2065–2076

    Article  Google Scholar 

  • Shan C, Zhang S, Ou X (2018) The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. Protoplasma. https://doi.org/10.1007/s00709-018-1213-5

    Article  PubMed  Google Scholar 

  • Shi H, Ye T, Chan Z (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71:226–234

    Article  CAS  Google Scholar 

  • Silva J, Kim YJ, Sukweenadhi J, Rahimi S, Kwon WS, Yang DC (2016) Molecular characterization of 5-chlorophyll a/b-binding protein genes from Panax ginseng Meyer and their expression analysis during abiotic stresses. Photosynthetica 54(3):446–458

    Article  CAS  Google Scholar 

  • Tai CH, Cook PF (2000) O-Acetylserine sulfhydrylase. Adv Enzymol Relat Areas Mol Biol 74:185–234

    CAS  Google Scholar 

  • Toit AD (2015) METABOLISM: the health benefits of hydrogen sulphide. Nat Rev Mol Cell Biol 16:68

    PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wang J, Ma XM, Kojima M, Sakakibara H, Hou BK (2011) N-Glucosyltransferase UGT76C2 is involved in cytokinin homeostasis and cytokinin response in Arabidopsis thaliana. Plant Cell Physiol 52(12):2200–2213

    Article  CAS  Google Scholar 

  • Wang RK, Cao ZH, Hao YJ (2014) Overexpression of a R2R3 MYB gene MdSIMYB1 increases tolerance to multiple stresses in transgenic tobacco and apples. Physiol Plant 150:76–87

    Article  CAS  Google Scholar 

  • Xie Y, Zhang C, Lai D, Sun Y, Samma MK, Zhang J, Shen W (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

    Article  CAS  Google Scholar 

  • Yadav K, Patel P, Srivastava AK, Ganapathi TR (2017) Overexpression of native ferritin gene MusaFer1 enhances iron content and oxidative stress tolerance in transgenic banana plants. PLoS ONE 12(11):e0188933

    Article  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14

    Article  Google Scholar 

  • Zang X, Geng X, Wang F, Liu Z, Zhang L, Zhao Y, Tian X, Ni Z, Yao Y, Xin M, Hu Z, Sun Q, Peng H (2017) Overexpression of wheat ferritin gene TaFER-5B enhances tolerance to heat stress and other abiotic stresses associated with the ROS scavenging. BMC Plant Biol 17:14

    Article  Google Scholar 

  • Zarei A, Korbes AP, Younessi P, Montiel G, Champion A, Memelink J (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol Biol 75:321–331

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhang H, Hu SL, Zhang ZJ, Hu LY, Jiang CX, Wei ZJ, Liu J, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257

    Article  CAS  Google Scholar 

  • Zheng Y, Jiao C, Sun H, Rosli HG, Pombo MA, Zhang P, Banf M, Dai X, Martin GB, Giovannoni JJ, Zhao PX, Rhee SY, Fei Z (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9:1667–1670

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by Science and Technology Project of Higher Education in Shandong Province (Grant No. J14LE12), Research Foundation for Advanced Talents of Qingdao Agricultural University, and National Natural Science Foundation of China (Grant No. 31540090).

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  1. Shandong Key Laboratory of Plant Biotechnology, College of Life Sciences, Qingdao Agricultural University, Qingdao, 266109, People’s Republic of China

    Qian Ma & Jingli Yang

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Correspondence to Qian Ma.

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Electronic supplementary material

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Supplementary material 1: The grapevine gene annotation information in this research. (XLS 41196 KB)

Supplementary material 2: The sequence templates used in qRT-PCR. (DOCX 25 KB)

Supplementary material 3: Oligonucleotide primers used in this study. (DOCX 19 KB)

13258_2018_723_MOESM4_ESM.tif

Supplementary material 4: The FPKM density distribution of H2S treated (H2S) and untreated grapevine plantlets in tissue culture (CTR). In figure, the X-axis number was calculated by log10(FPKM+1), and the Y-axis represented the gene density. (TIF 89 KB)

13258_2018_723_MOESM5_ESM.tif

Supplementary material 5: The volcano plot of differentially expressed genes with adjusted p-value <0.05 after H2S treatment. The X-axis indicated the log fold change of genes after H2S treatment, and the Y-axis showed the significant differences of gene expression. The highly expressed genes were represented by red spots, and the lowly regulated genes were denoted by green spots in the figure. (TIF 90 KB)

13258_2018_723_MOESM6_ESM.tif

Supplementary material 6: The volcano plot of differentially expressed genes with adjusted p-value <0.05, fold change >2, and the average FPKM >1 after H2S treatment. The highly expressed genes were panted by red color, and the lowly regulated genes were painted by green. (TIF 97 KB)

Supplementary material 7: The up-regulated genes after H2S treatment. (XLS 34 KB)

Supplementary material 8: The down-regulated genes after H2S treatment. (XLS 66 KB)

Supplementary material 9: The GO annotation of up-regulated DEGs used for functional enrichment analysis. (XLS 189 KB)

13258_2018_723_MOESM10_ESM.xls

Supplementary material 10: The KEGG annotation of up-regulated DEGs used for functional enrichment analysis. (XLS 58 KB)

13258_2018_723_MOESM11_ESM.xls

Supplementary material 11: The GO annotation of down-regulated DEGs used for functional enrichment analysis. (XLS 456 KB)

13258_2018_723_MOESM12_ESM.xls

Supplementary material 12: The KEGG annotation of down-regulated DEGs used for functional enrichment analysis. (XLS 54 KB)

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Ma, Q., Yang, J. Transcriptome profiling and identification of functional genes involved in H2S response in grapevine tissue cultured plantlets. Genes Genom 40, 1287–1300 (2018). https://doi.org/10.1007/s13258-018-0723-z

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