{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T02:43:29Z","timestamp":1791859409534,"version":"4.3.4"},"reference-count":64,"publisher":"Frontiers Media SA","content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"DOI":"10.3389\/fpls.2016.01173","type":"journal-article","created":{"date-parts":[[2016,8,3]],"date-time":"2016-08-03T23:06:49Z","timestamp":1470265609000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":127,"title":["Hydrogen Sulfide-Mediated Polyamines and Sugar Changes Are Involved in Hydrogen Sulfide-Induced Drought Tolerance in Spinacia oleracea Seedlings"],"prefix":"10.3389","volume":"7","author":[{"given":"Juan","family":"Chen","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Ting","family":"Shang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Hua","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xi-Yan","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"En-Ming","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hai-Lei","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhouping","family":"Shangguan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2016,8,4]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1007\/s00425-010-1130-0","article-title":"Polyamines: molecules with regulatory functions in plant abiotic stress tolerance.","volume":"231","author":"Alc\u00e1zar","year":"2010a","journal-title":"Planta"},{"key":"B2","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1016\/j.plaphy.2010.02.002","article-title":"Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene.","volume":"48","author":"Alc\u00e1zar","year":"2010b","journal-title":"Plant Physiol. Biochem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1337","DOI":"10.1046\/j.1365-3040.2001.00778.x","article-title":"The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat.","volume":"24","author":"Alexieva","year":"2001","journal-title":"Plant Cell Environ."},{"key":"B4","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1007\/BF00018060","article-title":"Rapid determination of free proline for water-stress studies.","volume":"39","author":"Bates","year":"1973","journal-title":"Plant Soil"},{"key":"B5","doi-asserted-by":"publisher","first-page":"3718","DOI":"10.1021\/jf990031h","article-title":"A single-step purification for glycine betaine determination in plant extracts by isocratic HPLC.","volume":"47","author":"Bessieres","year":"1999","journal-title":"J. Agric. Food. Chem."},{"key":"B6","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1007\/BF00024010","article-title":"Crop responses to drought and the interpretation of adaptation.","volume":"20","author":"Blum","year":"1996","journal-title":"Plant Growth Regul."},{"key":"B7","doi-asserted-by":"publisher","first-page":"9909","DOI":"10.1073\/pnas.0306974101","article-title":"Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress.","volume":"101","author":"Capell","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B8","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1071\/FP02076","article-title":"Understanding plant responses to drought \u2013 from genes to the whole plant.","volume":"30","author":"Chaves","year":"2003","journal-title":"Funct. Plant Biol."},{"issue":"12516","key":"B9","doi-asserted-by":"publisher","DOI":"10.1038\/srep12516","article-title":"Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots.","volume":"5","author":"Chen","year":"2015a","journal-title":"Sci. Rep."},{"key":"B10","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1007\/s11104-012-1275-7","article-title":"Hydrogen sulfide alleviates aluminum toxicity in barley seedlings.","volume":"362","author":"Chen","year":"2013","journal-title":"Plant Soil"},{"key":"B11","doi-asserted-by":"publisher","first-page":"6605","DOI":"10.1093\/jxb\/erv368","article-title":"Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency.","volume":"66","author":"Chen","year":"2015b","journal-title":"J. Exp. Bot."},{"key":"B12","doi-asserted-by":"publisher","first-page":"4481","DOI":"10.1093\/jxb\/err145","article-title":"Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings.","volume":"62","author":"Chen","year":"2011","journal-title":"J. Exp. Bot."},{"key":"B13","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1093\/jxb\/32.1.93","article-title":"Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase.","volume":"32","author":"Dhindsa","year":"1981","journal-title":"J. Exp. Bot."},{"key":"B14","doi-asserted-by":"publisher","first-page":"1620","DOI":"10.1016\/j.jplph.2007.11.006","article-title":"Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance.","volume":"165","author":"Duan","year":"2008","journal-title":"J. Plant Physiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"701","DOI":"10.1104\/pp.69.3.701","article-title":"Analysis of polyamines in higher plants by high performance liquid chromatography.","volume":"69","author":"Flores","year":"1982","journal-title":"Plant Physiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1196","DOI":"10.1104\/pp.126.3.1196","article-title":"Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress.","volume":"126","author":"Garc\u00eda-Mata","year":"2001","journal-title":"Plant Physiol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1111\/j.1469-8137.2010.03465.x","article-title":"Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling.","volume":"188","author":"Garc\u00eda-Mata","year":"2010","journal-title":"New Phytol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"15898","DOI":"10.1073\/pnas.252637799","article-title":"Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses.","volume":"99","author":"Garg","year":"2002","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B19","doi-asserted-by":"publisher","first-page":"6385","DOI":"10.1093\/jxb\/erv352","article-title":"High night temperature strongly impacts TCA cycle, amino acid and polyamine biosynthetic pathways in rice in a sensitivity-dependent manner.","volume":"66","author":"Glaubitz","year":"2015","journal-title":"J. Exp. Bot."},{"key":"B20","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1006\/bbrc.1997.6878","article-title":"The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide.","volume":"237","author":"Hosoki","year":"1997","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B21","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1016\/j.bbrc.2011.09.090","article-title":"Hydrogen sulfide improves drought resistance in Arabidopsis thaliana.","volume":"414","author":"Jin","year":"2011","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B22","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.plaphy.2012.10.017","article-title":"Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis.","volume":"62","author":"Jin","year":"2013","journal-title":"Plant Physiol. Biochem."},{"key":"B23","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1111\/j.0031-9317.2004.00309.x","article-title":"Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana.","volume":"121","author":"Kasinathan","year":"2004","journal-title":"Physiol. Plant"},{"key":"B24","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1146\/annurev.pp.42.060191.001525","article-title":"Chlorophyll fluorescence and photosynthesis: the basics.","volume":"42","author":"Krause","year":"1991","journal-title":"Annu. Rev. Plant Biol."},{"key":"B25","first-page":"354","article-title":"Effects of exogenous hydrogen sulfide (H2S) on the root tip and root border cells of Pisum sativum.","volume":"45","author":"Li","year":"2010","journal-title":"Chin. Bull. Bot."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s11738-015-1975-8","article-title":"Effect of hydrogen sulfide on D1 protein in wheat under drought stress.","volume":"37","author":"Li","year":"2015","journal-title":"Acta Physiol. Plant"},{"key":"B27","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1016\/j.coph.2005.10.007","article-title":"Hydrogen sulphide \u2013 a novel mediator of inflammation?","volume":"6","author":"Li","year":"2006","journal-title":"Curr. Opin. Pharmacol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using teal-time quantitative PCR and the 2-\u0394\u0394Ct method.","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"B29","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.jplph.2014.12.010","article-title":"Wounding induces changes in tuber polyamine content, polyamine metabolic gene expression, and enzyme activity during closing layer formation and initiation of wound periderm formation.","volume":"176","author":"Lulai","year":"2015","journal-title":"J. Plant Physiol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"5003","DOI":"10.1093\/jxb\/ers202","article-title":"The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants.","volume":"63","author":"Moschou","year":"2012","journal-title":"J. Exp. Bot."},{"key":"B31","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/j.plaphy.2015.01.009","article-title":"Water availability influences morphology, mycorrhizal associations, PSII efficiency and polyamine metabolism at early growth phase of Scots pine seedlings.","volume":"88","author":"Muilu-Makela","year":"2015","journal-title":"Plant Physiol. Biochem."},{"key":"B32","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/j.envexpbot.2008.09.009","article-title":"Leaf photosynthesis of Haberlea rhodopensis before and during drought.","volume":"65","author":"Peeva","year":"2009","journal-title":"Environ. Exp. Bot."},{"issue":"70","key":"B33","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2011.00070","article-title":"Trehalose-6-Phosphate: connecting plant metabolism and development.","volume":"2","author":"Ponnu","year":"2011","journal-title":"Front. Plant Sci."},{"key":"B34","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1093\/oxfordjournals.aob.a085354","article-title":"Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used.","volume":"41","author":"Prioul","year":"1977","journal-title":"Ann. Bot."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1059","DOI":"10.1111\/pce.12199","article-title":"The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants.","volume":"37","author":"Rivero","year":"2014","journal-title":"Plant Cell Environ."},{"key":"B36","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/S0168-9452(00)00388-5","article-title":"Tomato plant-water uptake and plant-water relationships under saline growth conditions.","volume":"160","author":"Romero-Aranda","year":"2001","journal-title":"Plant Sci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1104\/pp.70.2.430","article-title":"Emission of hydrogen sulfide by leaf tissue in response to L-cysteine.","volume":"70","author":"Sekiya","year":"1982","journal-title":"Plant Physiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"2533","DOI":"10.1007\/s11738-011-0746-4","article-title":"Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress.","volume":"33","author":"Shan","year":"2011","journal-title":"Acta Physiol. Plant"},{"key":"B39","doi-asserted-by":"publisher","first-page":"914","DOI":"10.1093\/treephys\/tpq030","article-title":"Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response.","volume":"30","author":"Shi","year":"2010","journal-title":"Tree Physiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/aob\/mcp259","article-title":"Polyamines: ubiquitous polycations with unique roles in growth and stress responses.","volume":"105","author":"Takahashi","year":"2010","journal-title":"Ann. Bot."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00425-014-2055-9","article-title":"The roles of polyamines during the lifespan of plants: from development to stress.","volume":"240","author":"Tiburcio","year":"2014","journal-title":"Planta"},{"key":"B42","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1016\/j.jplph.2009.10.022","article-title":"Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine.","volume":"167","author":"Toumi","year":"2010","journal-title":"J. Plant Physiol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1093\/pcp\/pci252","article-title":"Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings.","volume":"47","author":"Tun","year":"2006","journal-title":"Plant Cell Physiol."},{"key":"B44","first-page":"2895","article-title":"Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants.","volume":"84","author":"Wang","year":"1990","journal-title":"Plant Physiol. Commun."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1301","DOI":"10.1007\/s00425-010-1134-9","article-title":"Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings.","volume":"231","author":"Wang","year":"2010","journal-title":"Planta"},{"key":"B46","doi-asserted-by":"publisher","first-page":"1792","DOI":"10.1096\/fj.02-0211hyp","article-title":"Two\u2019s company, three\u2019s a crowd: can H2S be the third endogenous gaseous transmitter?","volume":"16","author":"Wang","year":"2002","journal-title":"FASEB J."},{"key":"B47","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/s11104-011-0936-2","article-title":"Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway.","volume":"351","author":"Wang","year":"2012","journal-title":"Plant Soil"},{"key":"B48","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1007\/s11248-007-9098-7","article-title":"Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers.","volume":"17","author":"Wen","year":"2008","journal-title":"Transgenic Res."},{"key":"B49","doi-asserted-by":"publisher","first-page":"627","DOI":"10.2307\/2389925","article-title":"Physiological responses of leaves of Rumex obtusifolius to damage by a leaf miner.","volume":"8","author":"Whittaker","year":"1994","journal-title":"Funct. Ecol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1111\/j.1365-3040.2009.02052.x","article-title":"Drought, ozone, ABA and ethylene: new insights from cell to plant to community.","volume":"33","author":"Wilkinson","year":"2010","journal-title":"Plant Cell Environ."},{"key":"B51","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1016\/j.tplants.2006.09.009","article-title":"NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants?","volume":"11","author":"Yamasaki","year":"2006","journal-title":"Trends Plant Sci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1126\/science.1162667","article-title":"H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine \u03b3 \u2013Lyase.","volume":"322","author":"Yang","year":"2008","journal-title":"Science"},{"key":"B53","doi-asserted-by":"publisher","first-page":"3099","DOI":"10.1007\/s11738-013-1343-5","article-title":"Application of silicon improves salt tolerance through ameliorating osmotic and ionic stresses in the seedling of Sorghum bicolor.","volume":"35","author":"Yin","year":"2013","journal-title":"Acta Physiol. Plant"},{"key":"B54","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1016\/j.plaphy.2014.04.014","article-title":"Silicon-mediated changes in polyamine and 1-aminocyclopropane-1-carboxylic acid are involved in silicon-induced drought resistance in Sorghum bicolor L.","volume":"80","author":"Yin","year":"2014","journal-title":"Plant Physiol. Biochem."},{"key":"B55","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1111\/pce.12521","article-title":"Silicon-mediated changes in polyamines participate in silicon-induced salt tolerance in Sorghum bicolor L.","volume":"39","author":"Yin","year":"2015","journal-title":"Plant Cell Environ."},{"key":"B56","doi-asserted-by":"publisher","first-page":"4128","DOI":"10.1105\/tpc.110.078691","article-title":"The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1.","volume":"22","author":"Yoo","year":"2010","journal-title":"Plant Cell"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1518","DOI":"10.1111\/j.1744-7909.2008.00769.x","article-title":"Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress.","volume":"50","author":"Zhang","year":"2008","journal-title":"J. Integr. Plant Biol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1016\/j.postharvbio.2011.01.006","article-title":"Hydrogen sulfide acts as a regulator of flower senescence in plants.","volume":"60","author":"Zhang","year":"2011","journal-title":"Postharvest Biol. Technol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"849","DOI":"10.1007\/s11738-010-0469-y","article-title":"Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress.","volume":"32","author":"Zhang","year":"2010a","journal-title":"Acta Physiol. Plant"},{"key":"B60","doi-asserted-by":"publisher","first-page":"556","DOI":"10.1111\/j.1744-7909.2010.00946.x","article-title":"Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings.","volume":"52","author":"Zhang","year":"2010b","journal-title":"J. Integr. Plant Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1007\/s10725-009-9372-1","article-title":"Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress.","volume":"58","author":"Zhang","year":"2009","journal-title":"Plant Growth Regul."},{"key":"B62","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1111\/j.1399-3054.2004.00367.x","article-title":"Expression of the maize GALACTINOL SYNTHASE gene family: (I) Expression of two different genes during seed development and germination.","volume":"121","author":"Zhao","year":"2004","journal-title":"Physiol. Plant"},{"key":"B63","doi-asserted-by":"publisher","first-page":"6008","DOI":"10.1093\/emboj\/20.21.6008","article-title":"The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener.","volume":"20","author":"Zhao","year":"2001","journal-title":"EMBO J."},{"key":"B64","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1007\/s11103-015-0379-x","article-title":"Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants.","volume":"89","author":"Ziogas","year":"2015","journal-title":"Plant Mol. Biol."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"deposited":{"date-parts":[[2017,6,24]],"date-time":"2017-06-24T15:54:43Z","timestamp":1498319683000},"score":1,"resource":{"primary":{"URL":"http:\/\/journal.frontiersin.org\/Article\/10.3389\/fpls.2016.01173\/abstract"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,8,4]]},"references-count":64,"URL":"https:\/\/doi.org\/10.3389\/fpls.2016.01173","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,8,4]]}}}