{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T12:48:39Z","timestamp":1789735719415,"version":"4.0.1"},"reference-count":73,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,6,1]],"date-time":"2017-06-01T00:00:00Z","timestamp":1496275200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,6,1]],"date-time":"2017-06-01T00:00:00Z","timestamp":1496275200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>There is growing evidence that hydrogen sulfide (H<jats:sub>2<\/jats:sub>S) is involved in many physiological processes in plants, but the role of H<jats:sub>2<\/jats:sub>S in dark-induced leaf senescence remains unknown. In this work, we found that H<jats:sub>2<\/jats:sub>S not only inhibited chlorophyll degradation but also caused the accumulation of photoreactive pheide <jats:italic>a<\/jats:italic> in detached leaves under extended darkness. Despite this, transcript levels of <jats:italic>senescence-associated genes<\/jats:italic> (<jats:italic>SAGs<\/jats:italic>) were less affected in H<jats:sub>2<\/jats:sub>S-treated detached leaves compared with those in H<jats:sub>2<\/jats:sub>S-untreated detached leaves. Furthermore, cell death\/rapid bleaching occurred in both H<jats:sub>2<\/jats:sub>S-treated detached and attached leaves after transfer from extended darkness to light. Unlike the lack of effect of H<jats:sub>2<\/jats:sub>S on <jats:italic>SAG<\/jats:italic> transcripts in darkened detached leaves, exogenous H<jats:sub>2<\/jats:sub>S induced higher SAG transcript levels in attached leaves than untreated attached leaves. Genetic evidence further underlined the positive correlation between SAG expression in attached leaves and H<jats:sub>2<\/jats:sub>S. In addition, effects of H<jats:sub>2<\/jats:sub>S on SAG expression in attached leaves were compromised in the <jats:italic>S<\/jats:italic>-nitrosoglutathione reductase-deficient mutant, <jats:italic>gsnor1<\/jats:italic>. Taken together, our results suggest that H<jats:sub>2<\/jats:sub>S suppresses chlorophyll degradation of detached leaves by regulating a dark-dependent reaction, and that this gas positively modulates SAG expression in attached leaves under prolonged darkness in a GSNOR1-dependent manner.<\/jats:p>","DOI":"10.1038\/s41598-017-02872-0","type":"journal-article","created":{"date-parts":[[2017,5,25]],"date-time":"2017-05-25T09:41:43Z","timestamp":1495705303000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":42,"title":["Functional analysis of the role of hydrogen sulfide in the regulation of dark-induced leaf senescence in Arabidopsis"],"prefix":"10.1038","volume":"7","author":[{"given":"Bo","family":"Wei","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Chao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianru","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tingting","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Graham","family":"Noctor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongsheng","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4424-1485","authenticated-orcid":false,"given":"Yi","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,6,1]]},"reference":[{"key":"2872_CR1","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1093\/toxsci\/65.1.18","volume":"65","author":"DC Dorman","year":"2002","unstructured":"Dorman, D. C. et al. Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci \n                           65, 18\u201325, doi:10.1093\/toxsci\/65.1.18 (2002).","journal-title":"Toxicol Sci"},{"key":"2872_CR2","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1093\/pcp\/pcu166","volume":"56","author":"H Birke","year":"2015","unstructured":"Birke, H., De Kok, L. J., Wirtz, M. & Hell, R. The role of compartment-specific cysteine synthesis for sulfur homeostasis during H2S exposure in Arabidopsis. Plant Cell Physiol \n                           56, 358\u2013367, doi:10.1093\/pcp\/pcu166 (2015).","journal-title":"Plant Cell Physiol"},{"key":"2872_CR3","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1104\/pp.61.2.184","volume":"61","author":"LG Wilson","year":"1978","unstructured":"Wilson, L. G., Bressan, R. A. & Filner, P. Light-dependent emission of hydrogen sulfide from plants. Plant Physiol \n                           61, 184\u2013189, doi:10.1104\/pp.61.2.184 (1978).","journal-title":"Plant Physiol"},{"key":"2872_CR4","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1104\/pp.70.2.430","volume":"70","author":"J Sekiya","year":"1982","unstructured":"Sekiya, J., Schmidt, A., Wilson, L. G. & Filner, P. Emission of Hydrogen Sulfide by Leaf Tissue in Response to L-Cysteine. Plant Physiol \n                           70, 430\u2013436, doi:10.1104\/pp.70.2.430 (1982).","journal-title":"Plant Physiol"},{"key":"2872_CR5","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1104\/pp.70.2.437","volume":"70","author":"J Sekiya","year":"1982","unstructured":"Sekiya, J., Wilson, L. G. & Filner, P. Resistance to injury by sulfur dioxide: correlation with its reduction to, and emission of, hydrogen sulfide in Cucurbitaceae. Plant Physiol \n                           70, 437\u2013441, doi:10.1104\/pp.70.2.437 (1982).","journal-title":"Plant Physiol"},{"key":"2872_CR6","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1016\/j.niox.2014.02.005","volume":"41","author":"A Calderwood","year":"2014","unstructured":"Calderwood, A. & Kopriva, S. Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide \n                           41, 72\u201378, doi:10.1016\/j.niox.2014.02.005 (2014).","journal-title":"Nitric Oxide"},{"key":"2872_CR7","doi-asserted-by":"publisher","first-page":"2305","DOI":"10.1093\/jxb\/erh236","volume":"55","author":"E Bloem","year":"2004","unstructured":"Bloem, E. et al. Sulphur supply and infection with Pyrenopezizabrassicae influence L-cysteine desulphydrase activity in Brassica napus L. J Exp Bot \n                           55, 2305\u20132312, doi:10.1093\/jxb\/erh236 (2004).","journal-title":"J Exp Bot"},{"key":"2872_CR8","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1016\/j.bbrc.2011.09.090","volume":"414","author":"Z Jin","year":"2011","unstructured":"Jin, Z. et al. Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun \n                           414, 481\u2013486, doi:10.1016\/j.bbrc.2011.09.090 (2011).","journal-title":"Biochem Biophys Res Commun"},{"key":"2872_CR9","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1104\/pp.109.147975","volume":"152","author":"C \u00c1lvarez","year":"2010","unstructured":"\u00c1lvarez, C., Calo, L., Romero, L. C., Garc\u00eda, I. & Gotor, C. An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol \n                           152, 656\u2013669, doi:10.1104\/pp.109.147975 (2010).","journal-title":"Plant Physiol"},{"key":"2872_CR10","doi-asserted-by":"publisher","first-page":"1617","DOI":"10.1073\/pnas.72.4.1617","volume":"72","author":"TN Akopyan","year":"1975","unstructured":"Akopyan, T. N., Braunstein, A. E. & Goryachenkova, E. V. Beta-cyanoalanine synthase: purification and characterization. Proc Natl Acad Sci USA \n                           72, 1617\u20131621, doi:10.1073\/pnas.72.4.1617 (1975).","journal-title":"Proc Natl Acad Sci USA"},{"key":"2872_CR11","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1104\/pp.123.3.1163","volume":"123","author":"Hatzfeld.","year":"2000","unstructured":"Hatzfeld. et al. beta-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol \n                           123, 1163\u20131171, doi:10.1104\/pp.123.3.1163 (2000).","journal-title":"Plant Physiol"},{"key":"2872_CR12","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1111\/j.1742-4658.2005.04567.x","volume":"272","author":"A Riemenschneider","year":"2005","unstructured":"Riemenschneider, A., Wegele, R., Schmidt, A. & Papenbrock, J. Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J \n                           272, 1291\u20131304, doi:10.1111\/j.1742-4658.2005.04567.x (2005).","journal-title":"FEBS J"},{"key":"2872_CR13","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.niox.2016.04.002","volume":"55\u201356","author":"H Yamasaki","year":"2016","unstructured":"Yamasaki, H. & Cohen, M. F. Biological consilience of hydrogen sulfide and nitric oxide in plants: Gases of primordial earth linking plant, microbial and animal physiologies. Nitric Oxide \n                           55\u201356, 91\u2013100, doi:10.1016\/j.niox.2016.04.002 (2016).","journal-title":"Nitric Oxide"},{"key":"2872_CR14","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1016\/j.plantsci.2012.11.007","volume":"201\u2013202","author":"C Garc\u00eda-Mata","year":"2013","unstructured":"Garc\u00eda-Mata, C. & Lamattina, L. Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci \n                           201\u2013202, 66\u201373, doi:10.1016\/j.plantsci.2012.11.007 (2013).","journal-title":"Plant Sci"},{"key":"2872_CR15","doi-asserted-by":"publisher","first-page":"609","DOI":"10.4161\/auto.23460","volume":"9","author":"C Gotor","year":"2013","unstructured":"Gotor, C., Garc\u00eda, I., Crespo, J. L. & Romero, L. C. Sulfide as a signaling molecule in autophagy. Autophagy \n                           9, 609\u2013611, doi:10.4161\/auto.23460 (2013).","journal-title":"Autophagy"},{"key":"2872_CR16","doi-asserted-by":"publisher","first-page":"1607","DOI":"10.1111\/pce.12073","volume":"36","author":"M Lisjak","year":"2013","unstructured":"Lisjak, M., Teklic, T., Wilson, I. D., Whiteman, M. & Hancock, J. T. Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ \n                           36, 1607\u20131616, doi:10.1111\/pce.2013.36.issue-9 (2013).","journal-title":"Plant Cell Environ"},{"key":"2872_CR17","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.plaphy.2014.02.012","volume":"78","author":"JT Hancock","year":"2014","unstructured":"Hancock, J. T. & Whiteman, M. Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol Biochem \n                           78, 37\u201342, doi:10.1016\/j.plaphy.2014.02.012 (2014).","journal-title":"Plant Physiol Biochem"},{"key":"2872_CR18","doi-asserted-by":"crossref","unstructured":"Jin, Z. & Pei, Y. Physiological implications of hydrogen sulfide in plants: pleasant exploration behind its unpleasant odour. Oxid Med Cell Longev 397502 (2015).","DOI":"10.1155\/2015\/397502"},{"key":"2872_CR19","doi-asserted-by":"publisher","first-page":"1518","DOI":"10.1111\/j.1744-7909.2008.00769.x","volume":"50","author":"H Zhang","year":"2008","unstructured":"Zhang, H. et al. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol \n                           50, 1518\u20131529, doi:10.1111\/jipb.2008.50.issue-12 (2008).","journal-title":"J Integr Plant Biol"},{"key":"2872_CR20","doi-asserted-by":"publisher","first-page":"1086","DOI":"10.1111\/j.1744-7909.2009.00885.x","volume":"51","author":"H Zhang","year":"2009","unstructured":"Zhang, H. et al. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol \n                           51, 1086\u20131094, doi:10.1111\/jipb.2009.51.issue-12 (2009).","journal-title":"J Integr Plant Biol"},{"key":"2872_CR21","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1016\/j.plaphy.2010.09.016","volume":"48","author":"M Lisjak","year":"2010","unstructured":"Lisjak, M. et al. A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem \n                           48, 931\u2013935, doi:10.1016\/j.plaphy.2010.09.016 (2010).","journal-title":"Plant Physiol Biochem"},{"key":"2872_CR22","doi-asserted-by":"publisher","first-page":"4481","DOI":"10.1093\/jxb\/err145","volume":"62","author":"J Chen","year":"2011","unstructured":"Chen, J. et al. Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinaciaoleracea seedlings. J Exp Bot \n                           62, 4481\u20134493, doi:10.1093\/jxb\/err145 (2011).","journal-title":"J Exp Bot"},{"key":"2872_CR23","doi-asserted-by":"publisher","first-page":"e62048","DOI":"10.1371\/journal.pone.0062048","volume":"8","author":"FD Dooley","year":"2013","unstructured":"Dooley, F. D., Nair, S. P. & Ward, P. D. Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One \n                           8, e62048, doi:10.1371\/journal.pone.0062048 (2013).","journal-title":"PLoS One"},{"key":"2872_CR24","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1111\/jipb.12004","volume":"5","author":"Z Hou","year":"2013","unstructured":"Hou, Z., Wang, L., Liu, J., Hou, L. & Liu, X. Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol \n                           5, 277\u2013289, doi:10.1111\/jipb.2013.55.issue-3 (2013).","journal-title":"J Integr Plant Biol"},{"key":"2872_CR25","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.plaphy.2013.12.024","volume":"76","author":"T Fang","year":"2014","unstructured":"Fang, T., Cao, Z., Li, J., Shen, W. & Huang, L. Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem \n                           76, 44\u201351, doi:10.1016\/j.plaphy.2013.12.024 (2014).","journal-title":"Plant Physiol Biochem"},{"key":"2872_CR26","doi-asserted-by":"publisher","first-page":"2065","DOI":"10.1104\/pp.114.245373","volume":"166","author":"D Scuffi","year":"2014","unstructured":"Scuffi, D. et al. Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol \n                           166, 2065\u20132076, doi:10.1104\/pp.114.245373 (2014).","journal-title":"Plant Physiol"},{"key":"2872_CR27","doi-asserted-by":"publisher","first-page":"8251","DOI":"10.1038\/srep08251","volume":"5","author":"H Jia","year":"2015","unstructured":"Jia, H., Hu, Y., Fan, T. & Li, J. Hydrogen sulfide modulates actin-dependent auxin transport via regulating ABPs results in changing of root development in Arabidopsis. Sci Rep \n                           5, 8251, doi:10.1038\/srep08251 (2015).","journal-title":"Sci Rep"},{"key":"2872_CR28","doi-asserted-by":"publisher","first-page":"930","DOI":"10.3389\/fpls.2016.00930","volume":"7","author":"E Baudouin","year":"2016","unstructured":"Baudouin, E. et al. The Significance of hydrogen sulfide for Arabidopsis seed germination. Front Plant Sci \n                           7, 930, doi:10.3389\/fpls.2016.00930 (2016).","journal-title":"Front Plant Sci"},{"key":"2872_CR29","doi-asserted-by":"publisher","first-page":"1301","DOI":"10.1007\/s00425-010-1134-9","volume":"231","author":"BL Wang","year":"2010","unstructured":"Wang, B. L., Shi, L., Li, Y. X. & Zhang, W. H. Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumissativus L.) seedlings. Planta \n                           231, 1301\u20131309, doi:10.1007\/s00425-010-1134-9 (2010).","journal-title":"Planta"},{"key":"2872_CR30","doi-asserted-by":"publisher","first-page":"1951","DOI":"10.1093\/jxb\/ert055","volume":"64","author":"A Christou","year":"2013","unstructured":"Christou, A., Manganaris, G. A., Papadopoulos, I. & Fotopoulos, V. 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 \n                           64, 1951\u20131953, doi:10.1093\/jxb\/ert055 (2013).","journal-title":"J Exp Bot"},{"key":"2872_CR31","doi-asserted-by":"publisher","first-page":"1564","DOI":"10.1111\/pce.12092","volume":"36","author":"ZG Li","year":"2013","unstructured":"Li, Z. G., Yang, S. Z., Long, W. B., Yang, G. X. & Shen, Z. Z. Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ \n                           36, 1564\u20131572, doi:10.1111\/pce.2013.36.issue-8 (2013).","journal-title":"Plant Cell Environ"},{"key":"2872_CR32","doi-asserted-by":"publisher","first-page":"e77047","DOI":"10.1371\/journal.pone.0077047","volume":"8","author":"J Shen.","year":"2013","unstructured":"Shen., J. et al. Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS One \n                           8, e77047, doi:10.1371\/journal.pone.0077047 (2013).","journal-title":"PLoS One"},{"key":"2872_CR33","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/j.plaphy.2013.07.021","volume":"71","author":"H Shi","year":"2013","unstructured":"Shi, H., Ye, T. & Chan, Z. Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodondactylon(L). Pers.). Plant Physiol Biochem \n                           71, 226\u2013234, doi:10.1016\/j.plaphy.2013.07.021 (2013).","journal-title":"Plant Physiol Biochem"},{"key":"2872_CR34","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.plaphy.2013.01.003","volume":"65","author":"J Sun","year":"2013","unstructured":"Sun, J. et al. Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populuseuphratica cells. Plant Physiol Biochem \n                           65, 67\u201374, doi:10.1016\/j.plaphy.2013.01.003 (2013).","journal-title":"Plant Physiol Biochem"},{"key":"2872_CR35","doi-asserted-by":"publisher","first-page":"12516","DOI":"10.1038\/srep12516","volume":"5","author":"J Chen","year":"2015","unstructured":"Chen, J. et al. Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep \n                           5, 12516, doi:10.1038\/srep12516 (2015).","journal-title":"Sci Rep"},{"key":"2872_CR36","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1007\/s11103-015-0379-x","volume":"89","author":"V Ziogas","year":"2015","unstructured":"Ziogas, V. et al. Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants. Plant Mol Biol \n                           89, 433\u2013450, doi:10.1007\/s11103-015-0379-x (2015).","journal-title":"Plant Mol Biol"},{"key":"2872_CR37","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1104\/pp.15.00009","volume":"168","author":"\u00c1 Aroca","year":"2015","unstructured":"Aroca, \u00c1., Serna, A., Gotor, C. & Romero, L. C. S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol \n                           168, 334\u2013342, doi:10.1104\/pp.15.00009 (2015).","journal-title":"Plant Physiol"},{"key":"2872_CR38","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1146\/annurev-arplant-042110-103921","volume":"62","author":"H Takahashi","year":"2011","unstructured":"Takahashi, H., Kopriva, S., Giordano, M., Saito, K. & Hell, R. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol \n                           62, 157\u2013184, doi:10.1146\/annurev-arplant-042110-103921 (2011).","journal-title":"Annu Rev Plant Biol"},{"key":"2872_CR39","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1146\/annurev.arplant.49.1.249","volume":"49","author":"G Noctor","year":"1998","unstructured":"Noctor, G. & Foyer, C. H. Ascorbate and Glutathione: Keeping active oxygen under control. Annu Rev Plant Biol \n                           49, 249\u2013279, doi:10.1146\/annurev.arplant.49.1.249 (1998).","journal-title":"Annu Rev Plant Biol"},{"key":"2872_CR40","doi-asserted-by":"publisher","first-page":"1144","DOI":"10.1104\/pp.110.153767","volume":"153","author":"A Mhamdi","year":"2010","unstructured":"Mhamdi, A. et al. Arabidopsis Glutathione Reductase1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol \n                           153, 1144\u20131160, doi:10.1104\/pp.110.153767 (2010).","journal-title":"Plant Physiol"},{"key":"2872_CR41","doi-asserted-by":"publisher","first-page":"2106","DOI":"10.1089\/ars.2012.5052","volume":"18","author":"Y Han","year":"2013","unstructured":"Han, Y. et al. Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid Redox Sign \n                           18, 2106\u20132121, doi:10.1089\/ars.2012.5052 (2013).","journal-title":"Antioxid Redox Sign"},{"key":"2872_CR42","doi-asserted-by":"publisher","first-page":"1135","DOI":"10.1111\/pce.12048","volume":"36","author":"Y Han","year":"2013","unstructured":"Han, Y., Mhamdi, A., Chaouch, S. & Noctor, G. Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant Cell Environ \n                           36, 1135\u20131146, doi:10.1111\/pce.2013.36.issue-6 (2013).","journal-title":"Plant Cell Environ"},{"key":"2872_CR43","doi-asserted-by":"publisher","first-page":"926","DOI":"10.1111\/tpj.12940","volume":"83","author":"MC Cheng","year":"2015","unstructured":"Cheng, M. C. et al. Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J \n                           83, 926\u2013939, doi:10.1111\/tpj.2015.83.issue-5 (2015).","journal-title":"Plant J"},{"key":"2872_CR44","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.1104\/pp.16.00110","volume":"171","author":"AM Laureano-Mar\u00edn","year":"2016","unstructured":"Laureano-Mar\u00edn, A. M., Moreno, I., Romero, L. C. & Gotor, C. Negative regulation of autophagy by sulfide is independent of Reactive Oxygen Species. Plant Physiol \n                           171, 1378\u20131391, doi:10.1104\/pp.16.00110 (2016).","journal-title":"Plant Physiol"},{"key":"2872_CR45","doi-asserted-by":"publisher","first-page":"4621","DOI":"10.1105\/tpc.112.105403","volume":"24","author":"C \u00c1lvarez","year":"2012","unstructured":"\u00c1lvarez, C. et al. Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell \n                           24, 4621\u20134634, doi:10.1105\/tpc.112.105403 (2012).","journal-title":"Plant Cell"},{"key":"2872_CR46","doi-asserted-by":"publisher","first-page":"2097","DOI":"10.1104\/pp.105.060673","volume":"138","author":"AR Thompson","year":"2005","unstructured":"Thompson, A. R., Doelling, J. H., Suttangkakul, A. & Vierstra, R. D. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol \n                           138, 2097\u20132110, doi:10.1104\/pp.105.060673 (2005).","journal-title":"Plant Physiol"},{"key":"2872_CR47","doi-asserted-by":"publisher","first-page":"2914","DOI":"10.1105\/tpc.109.068635","volume":"21","author":"K Yoshimoto","year":"2009","unstructured":"Yoshimoto, K. et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell \n                           21, 2914\u20132927, doi:10.1105\/tpc.109.068635 (2009).","journal-title":"Plant Cell"},{"key":"2872_CR48","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1111\/j.1365-3040.2011.02400.x","volume":"35","author":"G Noctor","year":"2012","unstructured":"Noctor, G. et al. Glutathione in plants: an integrated overview. Plant Cell Environ \n                           35, 454\u2013484, doi:10.1111\/j.1365-3040.2011.02400.x (2012).","journal-title":"Plant Cell Environ"},{"key":"2872_CR49","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1093\/mp\/sst168","volume":"7","author":"LC Romero","year":"2014","unstructured":"Romero, L. C. et al. Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant \n                           7, 264\u2013276, doi:10.1093\/mp\/sst168 (2014).","journal-title":"Mol Plant"},{"key":"2872_CR50","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1146\/annurev.arplant.57.032905.105316","volume":"58","author":"PO Lim","year":"2007","unstructured":"Lim, P. O., Kim, H. J. & Nam, H. G. Leaf senescence. Annu Rev Plant Biol \n                           58, 115\u2013136, doi:10.1146\/annurev.arplant.57.032905.105316 (2007).","journal-title":"Annu Rev Plant Biol"},{"key":"2872_CR51","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1104\/pp.115.2.669","volume":"115","author":"S Rodoni","year":"1997","unstructured":"Rodoni, S. et al. Chlorophyll breakdown in senescent chloroplasts (Cleavage of Pheophorbide a in Two Enzymic Steps. Plant Physiol \n                           115, 669\u2013676, doi:10.1104\/pp.115.2.669 (1997).","journal-title":"Plant Physiol"},{"key":"2872_CR52","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1104\/pp.105.065870","volume":"139","author":"A Pru\u017einsk\u00e1","year":"2005","unstructured":"Pru\u017einsk\u00e1, A. et al. Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol \n                           139, 52\u201363, doi:10.1104\/pp.105.065870 (2005).","journal-title":"Plant Physiol"},{"key":"2872_CR53","doi-asserted-by":"publisher","first-page":"15362","DOI":"10.1073\/pnas.96.26.15362","volume":"96","author":"T Tsuchiya","year":"1999","unstructured":"Tsuchiya, T. et al. Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA \n                           96, 15362\u201315367, doi:10.1073\/pnas.96.26.15362 (1999).","journal-title":"Proc Natl Acad Sci USA"},{"key":"2872_CR54","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1105\/tpc.106.044404","volume":"19","author":"A Pru\u017einsk\u00e1","year":"2007","unstructured":"Pru\u017einsk\u00e1, A. et al. In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell \n                           19, 369\u2013387, doi:10.1105\/tpc.106.044404 (2007).","journal-title":"Plant Cell"},{"key":"2872_CR55","doi-asserted-by":"publisher","first-page":"1429","DOI":"10.1104\/pp.107.100172","volume":"144","author":"G Ren","year":"2007","unstructured":"Ren, G. et al. Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol \n                           144, 1429\u20131441, doi:10.1104\/pp.107.100172 (2007).","journal-title":"Plant Physiol"},{"key":"2872_CR56","doi-asserted-by":"publisher","first-page":"17449","DOI":"10.1074\/jbc.M109.008912","volume":"284","author":"Y Horie","year":"2009","unstructured":"Horie, Y. et al. Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a\/b-protein complexes in Arabidopsis. J Biol Chem \n                           284, 17449\u201317456, doi:10.1074\/jbc.M109.008912 (2009).","journal-title":"J Biol Chem"},{"key":"2872_CR57","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.ab.2007.01.005","volume":"363","author":"G Queval","year":"2007","unstructured":"Queval, G. & Noctor, G. A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: Application to redox profiling during Arabidopsis rosette development. Anal. Biochem. \n                           363, 58\u201369, doi:10.1016\/j.ab.2007.01.005 (2007).","journal-title":"Anal. Biochem."},{"key":"2872_CR58","doi-asserted-by":"publisher","first-page":"3436","DOI":"10.1105\/tpc.105.037770","volume":"17","author":"FQ Guo","year":"2005","unstructured":"Guo, F. Q. & Crawford, N. M. Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell \n                           17, 3436\u20133450, doi:10.1105\/tpc.105.037770 (2005).","journal-title":"Plant Cell"},{"key":"2872_CR59","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1111\/j.1365-3040.2006.01604.x","volume":"30","author":"TE Mishina","year":"2007","unstructured":"Mishina, T. E., Lamb, C. & Zeier, J. Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ \n                           30, 39\u201352, doi:10.1111\/pce.2007.30.issue-1 (2007).","journal-title":"Plant Cell Environ"},{"key":"2872_CR60","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1038\/35055104","volume":"3","author":"SR Jaffrey","year":"2001","unstructured":"Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P. & Snyder, S. H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol \n                           3, 193\u2013197, doi:10.1038\/35055104 (2001).","journal-title":"Nat Cell Biol"},{"key":"2872_CR61","doi-asserted-by":"publisher","first-page":"8054","DOI":"10.1073\/pnas.0501456102","volume":"102","author":"A Feechan","year":"2005","unstructured":"Feechan, A. et al. A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA \n                           102, 8054\u20138059, doi:10.1073\/pnas.0501456102 (2005).","journal-title":"Proc Natl Acad Sci USA"},{"key":"2872_CR62","doi-asserted-by":"publisher","first-page":"1731","DOI":"10.1104\/pp.15.00026","volume":"167","author":"J Hu","year":"2015","unstructured":"Hu, J. et al. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol \n                           167, 1731\u20131746, doi:10.1104\/pp.15.00026 (2015).","journal-title":"Plant Physiol"},{"key":"2872_CR63","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1046\/j.1365-313x.2000.00836.x","volume":"23","author":"K Morris","year":"2000","unstructured":"Morris, K. et al. Salicylic acid has a role in regulating gene expression during leaf senescence. The Plant J \n                           23, 677\u2013685, doi:10.1046\/j.1365-313x.2000.00836.x (2000).","journal-title":"The Plant J"},{"key":"2872_CR64","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1111\/j.1469-8137.2011.03889.x","volume":"193","author":"C \u00c1lvarez","year":"2012","unstructured":"\u00c1lvarez, C., Berm\u00fadez, M. \u00c1., Romero, L. C., Gotor, C. & Garc\u00eda, I. Cysteine homeostasis plays an essential role in plant immunity. New Phytol \n                           193, 165\u2013177, doi:10.1111\/j.1469-8137.2011.03889.x (2012).","journal-title":"New Phytol"},{"key":"2872_CR65","doi-asserted-by":"publisher","first-page":"1321","DOI":"10.1104\/pp.110.157180","volume":"153","author":"A Smykowski","year":"2010","unstructured":"Smykowski, A., Zimmermann, P. & Zentgraf, U. G-Box binding factor1 reduces CATALASE2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiol \n                           153, 1321\u20131331, doi:10.1104\/pp.110.157180 (2010).","journal-title":"Plant Physiol"},{"key":"2872_CR66","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1007\/s00425-014-2209-9","volume":"241","author":"L Ma","year":"2015","unstructured":"Ma, L. et al. Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotata to altitude gradient in the Northern Tibetan Plateau. Planta \n                           241, 887\u2013906, doi:10.1007\/s00425-014-2209-9 (2015).","journal-title":"Planta"},{"key":"2872_CR67","doi-asserted-by":"publisher","first-page":"1766","DOI":"10.1104\/pp.113.222703","volume":"163","author":"MC de Pinto","year":"2013","unstructured":"de Pinto, M. C. et al. S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol \n                           163, 1766\u20131775, doi:10.1104\/pp.113.222703 (2013).","journal-title":"Plant Physiol"},{"key":"2872_CR68","doi-asserted-by":"publisher","first-page":"8868","DOI":"10.1074\/jbc.M709567200","volume":"283","author":"M Zaffagnini","year":"2008","unstructured":"Zaffagnini, M., Michelet, L., Massot, V., Trost, P. & Lemaire, S. D. Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J Biol Chem \n                           283, 8868\u20138876, doi:10.1074\/jbc.M709567200 (2008).","journal-title":"J Biol Chem"},{"key":"2872_CR69","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1046\/j.1365-313x.1998.00262.x","volume":"16","author":"CS Cobbett","year":"1998","unstructured":"Cobbett, C. S., May, M. J., Howden, R. & Rolls, B. The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. Plant J \n                           16, 73\u201378, doi:10.1046\/j.1365-313x.1998.00262.x (1998).","journal-title":"Plant J"},{"key":"2872_CR70","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.jplph.2015.03.015","volume":"181","author":"VP Singh","year":"2015","unstructured":"Singh, V. P., Singh, S., Kumar, J. & Prasad, S. M. Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: Possible involvement of nitric oxide. J Plant Physiol \n                           181, 20\u201329, doi:10.1016\/j.jplph.2015.03.015 (2015).","journal-title":"J Plant Physiol"},{"key":"2872_CR71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0008-6215(87)80114-3","volume":"164","author":"FWK Lichtenthaler","year":"1987","unstructured":"Lichtenthaler, F. W. K., Freudenberg, B. & Helferich, H. O. L. Fischer: a centennial tribute. Carbohydr Res \n                           164, 1\u201322 (1987).","journal-title":"Carbohydr Res"},{"key":"2872_CR72","doi-asserted-by":"publisher","first-page":"1140","DOI":"10.1111\/pce.12726","volume":"39","author":"G Noctor","year":"2016","unstructured":"Noctor, G., Mhamdi, A. & Foyer, C. H. Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ \n                           39, 1140\u20131160, doi:10.1111\/pce.v39.5 (2016).","journal-title":"Plant Cell Environ"},{"key":"2872_CR73","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1104\/pp.59.3.411","volume":"59","author":"T Brennan","year":"1977","unstructured":"Brennan, T. & Frenkel, C. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol \n                           59, 411\u2013416, doi:10.1104\/pp.59.3.411 (1977).","journal-title":"Plant Physiol"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-02872-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-02872-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-02872-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T04:47:31Z","timestamp":1671770851000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-02872-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,6,1]]},"references-count":73,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["2872"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-02872-0","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,6,1]]},"assertion":[{"value":"15 November 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 April 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 June 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"2615"}}