Abstract
Emerging evidence suggests that the gaseous molecules hydrogen sulfide (H2S) and nitric oxide (NO) enhances plant acclimation to stress; however, the underlying mechanism remains unclear. In this work, we explored if pretreatment of citrus roots with NaHS (a H2S donor) or sodium nitroprusside (SNP, a NO donor) for 2 days (d) could elicit long-lasting priming effects to subsequent exposure to PEG-associated drought stress for 21 d following a 5 d acclimation period. Detailed physiological study documented that both pretreatments primed plants against drought stress. Analysis of the level of nitrite, NOx, S-nitrosoglutahione reductase, Tyr-nitration and S-nitrosylation along with the expression of genes involved in NO-generation suggested that the nitrosative status of leaves and roots was altered by NaHS and SNP. Using a proteomic approach we characterized S-nitrosylated proteins in citrus leaves exposed to chemical treatments, including well known and novel S-nitrosylated targets. Mass spectrometry analysis also enabled the identification of 42 differentially expressed proteins in PEG alone-treated plants. Several PEG-responsive proteins were down-regulated, especially photosynthetic proteins. Finally, the identification of specific proteins that were regulated by NaHS and SNP under PEG conditions provides novel insight into long-term drought priming in plants and in a fruit crop such as citrus in particular.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abat JK, Saigal P, Deswal R (2008) S-Nitrosylation—another biological switch like phosphorylation? Physiol Mol Biol Plants 14:119–130. doi:10.1007/s12298-008-0011-5
Álvarez C, Calo L, Romero LC, García I, Gotor C (2010) An o-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669. doi:10.1104/pp.109.147975
Baudouin E, Hancock JT (2014) Nitric oxide signaling in plants. Front Plant Sci 4:553. doi:10.3389/fpls.2013.00553
Bevan M, Bancroft I, Bent E et al (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488. doi:10.1038/35140
Bloem E, Riemenschneider A, Volker J et al (2004) Sulphur supply and infection with Pyrenopeziza brassicae influence l-cysteine desulphydrase activity in Brassica napus L. J Exp Bot 55:2305–2312. doi:10.1093/jxb/erh236
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Chaki M, Valderrama R, Fernández-Ocaña AM et al (2011) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant, Cell Environ 34:1803–1818. doi:10.1111/j.1365-3040.2011.02376.x
Chen K, Chen L, Fan J, Fu J (2013) Alleviation of heat damage to photosystem II by nitric oxide in tall fescue. Photosynth Res 116:21–31. doi:10.1007/s11120-013-9883-5
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. doi:10.1093/jxb/ert055
Christou A, Filippou P, Manganaris G, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14:42. doi:10.1186/1471-2229-14-42
Corpas FJ, Chaki M, Fernández-Ocaña A et al (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722. doi:10.1093/pcp/pcn144
Deeba F et al (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol Biochem 53:6–18. doi:10.1016/j.plaphy.2012.01.002
Esechie A, Kiss L, Olah G, Horvath EM, Horvath E, Szabo C, Traber DL (2008) Protective effect of hydrogen sulfide in a murine model of acute lung injury induced by combined burn and smoke inhalation. Clin Sci 115:91–97. doi:10.1042/CS20080021
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449. doi:10.1038/nrm1492
Finkel T (2012) From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Sci Signal 5(215):pe10. doi:10.1126/scisignal.2002943
García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signaling. New Phytol 188:977–984. doi:10.1111/j.1469-8137.2010.03465.x
García-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201–202:66–73. doi:10.1016/j.plantsci.2012.11.007
García-Sánchez F, Syvertsen JP, Gimeno V, Botía P, Perez-Perez JG (2007) Responses to flooding and drought stress by two citrus rootstock seedlings with different water-use efficiency. Physiologia Plant 130:532–542. doi:10.1111/j.1399-3054.2007.00925.x
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151. doi:10.3389/fpls.2014.00151
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168. doi:10.1016/j.tplants.2010.11.007
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1
Igamberdiev AU, Bykova NV, Ens W, Hill RD (2004) Dihydrolipoamide dehydrogenase from porcine heart catalyzes NADH-dependent scavenging of nitric oxide. FEBS Lett 568:146–150. doi:10.1016/j.febslet.2004.05.024
Jaffrey SR, Snyder SH (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci Signal 86:pl1. doi:10.1126/stke.2001.86.pl1
Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486. doi:10.1016/j.bbrc.2011.09.090
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. doi:10.1016/j.plaphy.2012.10.017
Kabil O, Vitvitsky V, Banerjee R (2014) Sulfur as a signaling nutrient through hydrogen sulfide. Annu Rev Nutr 34:171–205. doi:10.1146/annurev-nutr-071813-105654
Kubo S, Kurokawa Y, Doe I, Masuko T, Sekiguchi F, Kawabata A (2007) Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 241:92–97. doi:10.1016/j.tox.2007.08.087
Kurek I, Stoger E, Dulberger R, Christou P, Breiman A (2002) Overexpression of the wheat FK506-binding protein 73 (FKBP73) and the heat-induced wheat FKBP77 in transgenic wheat reveals different functions of the two isoforms. Transgenic Res 11:373–379. doi:10.1007/s00438-008-0318-5
Leterrier M, Barroso JB, Palma JM, Corpas FJ (2012) Cytosolic NADP-isocitrate dehydrogenase in Arabidopsis leaves and roots. Biol Plant 56:705–710. doi:10.1007/s10535-012-0244-6
Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930. doi:10.1104/pp.104.058719
Lisjak M et al (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935. doi:10.1016/j.plaphy.2010.09.016
Lounifi I, Arc E, Molassiotis A, Job D, Rajjou L, Tanou G (2013) Interplay between protein carbonylation and nitrosylation in plants. Proteomics 13:568–578. doi:10.1002/pmic.201200304
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158. doi:10.1016/j.abb.2005.10.018
Mahe A, Grisvard J, Dron M (1992) Fungal and specific gene markers to follow the bean-anthracnose infection process and mormalize the bean chitinase rnRNA induction. Mol Plant Microbe Interact 5:242–248
Martínez MC, Achkor H, Persson B et al (1996) Arabidopsis formaldehyde dehydrogenase. Molecular properties of plant class III alcohol dehydrogenase provide further insights into the origins, structure and function of plant class P and liver class I alcohol dehydrogenases. Eur J Biochem 241:849–857. doi:10.1111/j.1432-1033.1996.00849.x
Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler RON (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. doi:10.1111/j.1365-3040.2009.02041.x
Molassiotis A, Fotopoulos V (2011) Oxidative and nitrosative signaling in plants: two branches in the same tree? Plant Signal Behav 6:210–214. doi:10.4161/psb.6.2.14878
Nashef AS, Osuga DT, Feeney RE (1977) Determination of hydrogen sulfide with 5,5′-dithiobis-(2-nitrobenzoic acid), N-ethylmaleimide, and parachloromercuribenzoate. Anal Biochem 79:394–405. doi:10.1016/0003-2697(77)90413-4
Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103. doi:10.1093/jxb/err414
Pandey S (2014) Hydrogen sulfide: a new node in the abscisic acid-dependent guard cell signaling network? Plant Physiol 166:1680–1681. doi:10.1104/pp.114.251686
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. doi:10.1093/nar/30.9.e36
Puyaubert J, Baudouin E (2014) New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ 37:2623–2630. doi:10.1111/pce.12329
Qiao Z, Jing T, Liu Z, Zhang L, Jin Z, Liu D, Pei Y (2015) H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant Soil 393:137–146. doi:10.1007/s11104-015-2475-8
Riccardi F, Gazeau P, de Vienne D, Zivy M (1998) Protein changes in response to progressive water deficit in maize: quantitative variation and polypeptide identification. Plant Physiol 117:1253–1263. doi:10.1104/pp.117.4.1253
Riemenschneider A, Nikiforova V, Hoefgen R, De Kok LJ, Papenbrock J (2005a) Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473–483. doi:10.1016/j.plaphy.2005.04.001
Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005b) Isolation and characterization of a d-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272:1291–1304. doi:10.1111/j.1742-4658.2005.04567.x
Rizhsky L et al (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342. doi:10.1046/j.1365-313X.2002.01427.x
Rümer S, Krischke M, Fekete A, Mueller MJ, Kaiser WM (2012) DAF-fluorescence without NO: elicitor treated tobacco cells produce fluorescing DAF-derivatives not related to DAF-2 triazol. Nitric Oxide 27:123–135. doi:10.1016/j.niox.2012.05.007
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. doi:10.1104/pp.114.245373
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. doi:10.1371/journal.pone.0077047
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. doi:10.1016/j.plaphy.2013.07.021
Shi H, Ye T, Zhu J-K, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65:4119–4131. doi:10.1093/jxb/eru184
Taketani S, Adachi Y, Kohno H, Ikehara S, Tokunaga R, Ishii T (1998) Molecular characterization of a newly identified heme-binding protein induced during differentiation of urine erythroleukemia cells. J Biol Chem 273:31388–31394. doi:10.1074/jbc.273.47.31388
Tan BH, Wong PTH, Bian J-S (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3–10. doi:10.1016/j.neuint.2009.08.008
Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804. doi:10.1111/j.1365-313X.2009.04000.x
Tanou G, Job C, Belghazi M, Molassiotis A, Diamantidis G, Job D (2010) Proteomic signatures uncover hydrogen peroxide and nitric oxide cross-talk signaling network in citrus plants. J Proteome Res 9:5994–6006. doi:10.1021/pr100782h
Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012a) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599. doi:10.1111/j.1365-313X.2012.05100.x
Tanou G, Fotopoulos V, Molassiotis A (2012b) Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front Plant Sci 3:216. doi:10.3389/fpls.2012.00216
Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37:864–885. doi:10.1111/pce.12204
Valderrama R, Francisco JC, Carreras A et al (2007) Nitrosative stress in plants. FEBS Lett 581:453–461. doi:10.1016/j.febslet.2007.01.006
van Engelen FA, Hartog MV, Thomas TL, Taylor B, Sturm A, van Kammen A, de Vries SC (1993) The carrot secreted glycoprotein gene EP1 is expressed in the epidermis and has sequence homology to Brassica S-locus glycoproteins. Plant J 4:855–862. doi:10.1046/j.1365-313X.1993.04050855.x
Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896. doi:10.1152/physrev.00017.2011
Wang P, Du Y, Hou Y-J, Zhao Y, Hsu C-C, Yuan F, Zhu X, Tao WA, Song C-P, Zhu J-K (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci USA 112:613–618. doi:10.1073/pnas.1423481112
Whiteman M, Li L, Kostetski I, Chu SH, Siau JL, Bhatia M, Moore PK (2006) Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Biophys Res Commun 343:303–310. doi:10.1016/j.bbrc.2006.02.154
Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiol 61:184–189. doi:10.1104/pp.61.2.184
Wünsche H, Baldwin IT, Wu J (2011) S-Nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata. J Exp Bot 62:4605–4616. doi:10.1093/jxb/err171
Xiong L, Wang R-G, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol 142:1065–1074. doi:10.1104/pp.106.084632
Xu C, Jiang Z, Huang B (2011) Nitrogen deficiency-induced protein changes in immature and mature leaves of creeping bentgrass. J Am Soc Hortic Sci 136:399–407
Yu Y, Zhang H, Li W, Mu C, Zhang F, Wang L, Meng Z (2012) Genome-wide analysis and environmental response profiling of the FK506-binding protein gene family in maize (Zea mays L.). Gene 498:212–222. doi:10.1016/j.gene.2012.01.094
Zadražnik T, Hollung K, Egge-Jacobsen W, Meglič V, Šuštar-Vozlič J (2013) Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J Proteomics 78:254–272. doi:10.1016/j.jprot.2012.09.021
Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50. doi:10.1111/j.1469-8137.2007.02071.x
Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228. doi:10.1093/jxb/eri319
Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol Biochem 68:118–126. doi:10.1016/j.plaphy.2013.04.004
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ziogas, V., Tanou, G., Belghazi, M. et al. Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants. Plant Mol Biol 89, 433–450 (2015). https://doi.org/10.1007/s11103-015-0379-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-015-0379-x