{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,19]],"date-time":"2026-02-19T09:32:42Z","timestamp":1771493562447,"version":"3.50.1"},"reference-count":91,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2020,2,18]],"date-time":"2020-02-18T00:00:00Z","timestamp":1581984000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31501822"],"award-info":[{"award-number":["31501822"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Plant Cell &amp; Environment"],"published-print":{"date-parts":[[2020,5]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Hydrogen sulfide (H<jats:sub>2<\/jats:sub>S) is emerging as an important signalling molecule that regulates plant growth and abiotic stress responses. However, the roles of H<jats:sub>2<\/jats:sub>S in symbiotic nitrogen (N) assimilation and remobilization have not been characterized. Therefore, we examined how H<jats:sub>2<\/jats:sub>S influences the soybean (<jats:styled-content style=\"fixed-case\"><jats:italic>Glycine max<\/jats:italic><\/jats:styled-content>)\/rhizobia interaction in terms of symbiotic N fixation and mobilization during N deficiency\u2010induced senescence. H<jats:sub>2<\/jats:sub>S enhanced biomass accumulation and delayed leaf senescence through effects on nodule numbers, leaf chlorophyll contents, leaf N resorption efficiency, and the N contents in different tissues. Moreover, grain numbers and yield were regulated by H<jats:sub>2<\/jats:sub>S and rhizobia, together with N accumulation in the organs, and N use efficiency. The synergistic effects of H<jats:sub>2<\/jats:sub>S and rhizobia were also demonstrated by effects on the enzyme activities, protein abundances, and gene expressions associated with N metabolism, and senescence\u2010associated genes (<jats:italic>SAG<\/jats:italic>s) expression in soybeans grown under conditions of N deficiency. Taken together, these results show that H<jats:sub>2<\/jats:sub>S and rhizobia accelerate N assimilation and remobilization by regulation of the expression of <jats:italic>SAG<\/jats:italic>s during N deficiency\u2010induced senescence. Thus, H<jats:sub>2<\/jats:sub>S enhances the vegetative and reproductive growth of soybean, presumably through interactions with rhizobia under conditions of N deficiency.<\/jats:p>","DOI":"10.1111\/pce.13736","type":"journal-article","created":{"date-parts":[[2020,2,3]],"date-time":"2020-02-03T21:27:08Z","timestamp":1580765228000},"page":"1130-1147","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":39,"title":["Hydrogen sulfide and rhizobia synergistically regulate nitrogen (N) assimilation and remobilization during N deficiency\u2010induced senescence in soybean"],"prefix":"10.1111","volume":"43","author":[{"given":"Ni\u2010Na","family":"Zhang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau Northwest A &amp; F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hang","family":"Zou","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Stress Biology in Arid Areas, College of life sciences Northwest A&amp;F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xue\u2010Yuan","family":"Lin","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau Northwest A &amp; F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qing","family":"Pan","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Stress Biology in Arid Areas, College of life sciences Northwest A&amp;F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei\u2010Qin","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau Northwest A &amp; F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jian\u2010Hua","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Biology Hong Kong Baptist University  Kowloon Tong Hong Kong"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ge\u2010Hong","family":"Wei","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Crop Stress Biology in Arid Areas, College of life sciences Northwest A&amp;F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhou\u2010Ping","family":"Shangguan","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau Northwest A &amp; F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8395-3314","authenticated-orcid":false,"given":"Juan","family":"Chen","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau Northwest A &amp; F University  Yangling P.R. China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2020,2,18]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1134\/S1021443708010020"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/eru039"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0190269"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.00930"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1007\/s004250000355"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0923-2508(03)00029-9"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41477-018-0191-0"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.111.083345"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.95.4.997"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1022358016487"},{"issue":"12516","key":"e_1_2_7_12_1","first-page":"1173","article-title":"Hydrogen sulfide\u2010mediated polyamines and sugar changes are involved in hydrogen sulfide\u2010induced drought tolerance in Spinacia oleracea seedlings","volume":"7","author":"Chen J.","year":"2016","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1002\/jpln.201700262"},{"key":"e_1_2_7_14_1","doi-asserted-by":"publisher","DOI":"10.1038\/srep12516"},{"key":"e_1_2_7_15_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erv368"},{"key":"e_1_2_7_16_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/err145"},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00344-017-9704-8"},{"key":"e_1_2_7_18_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.10.5.741"},{"key":"e_1_2_7_19_1","doi-asserted-by":"publisher","DOI":"10.17221\/70\/2013-PSE"},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1002\/jpln.201700110"},{"key":"e_1_2_7_21_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.108.119040"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2013.12.024"},{"key":"e_1_2_7_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fcr.2013.09.003"},{"key":"e_1_2_7_24_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.113.2.313"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.106.079293"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.indcrop.2019.111513"},{"key":"e_1_2_7_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.2012.04084.x"},{"issue":"10","key":"e_1_2_7_28_1","first-page":"2513","article-title":"Nitrogen remobilization during leaf senescence: Lessons from Arabidopsis to crops","volume":"68","author":"Have M.","year":"2017","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1072831"},{"key":"e_1_2_7_30_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/eru094"},{"key":"e_1_2_7_31_1","doi-asserted-by":"publisher","DOI":"10.1006\/bbrc.1997.6878"},{"key":"e_1_2_7_32_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.postharvbio.2015.05.003"},{"key":"e_1_2_7_33_1","doi-asserted-by":"publisher","DOI":"10.1078\/0176-1617-01118"},{"key":"e_1_2_7_34_1","doi-asserted-by":"publisher","DOI":"10.1078\/0176-1617-01178"},{"key":"e_1_2_7_35_1","doi-asserted-by":"publisher","DOI":"10.1007\/s004250050260"},{"key":"e_1_2_7_36_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12892-015-0127-4"},{"key":"e_1_2_7_37_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.01722"},{"key":"e_1_2_7_38_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11104-017-3335-5"},{"key":"e_1_2_7_39_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erq297"},{"key":"e_1_2_7_40_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11356-018-1510-8"},{"key":"e_1_2_7_41_1","doi-asserted-by":"publisher","DOI":"10.1080\/01904167.2018.1485164"},{"key":"e_1_2_7_42_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.00044"},{"key":"e_1_2_7_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fcr.2016.06.015"},{"key":"e_1_2_7_44_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11738-016-2079-9"},{"key":"e_1_2_7_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.postharvbio.2017.03.017"},{"key":"e_1_2_7_46_1","doi-asserted-by":"publisher","DOI":"10.1021\/jf4047122"},{"issue":"9","key":"e_1_2_7_47_1","first-page":"1749","article-title":"Auxin response factor, GmARF10, positively regulates leaf senescence processes in Glycine max","volume":"34","author":"Li X. P.","year":"2014","journal-title":"Acta Botanica Boreali\u2010Occidentalia Sinica"},{"key":"e_1_2_7_48_1","doi-asserted-by":"publisher","DOI":"10.3390\/cells8010050"},{"key":"e_1_2_7_49_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0213874"},{"key":"e_1_2_7_50_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.arplant.57.032905.105316"},{"key":"e_1_2_7_51_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF03030735"},{"key":"e_1_2_7_52_1","doi-asserted-by":"publisher","DOI":"10.1006\/meth.2001.1262"},{"key":"e_1_2_7_53_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2015.00317"},{"key":"e_1_2_7_54_1","doi-asserted-by":"publisher","DOI":"10.1007\/s004250000310"},{"issue":"1","key":"e_1_2_7_55_1","first-page":"23","article-title":"Leaf nitrogen remobilisation for plant development and grain filling","volume":"10","author":"Masclauxdaubresse C.","year":"2010","journal-title":"Plant Biology"},{"key":"e_1_2_7_56_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2008.02.002"},{"key":"e_1_2_7_57_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erj035"},{"key":"e_1_2_7_58_1","doi-asserted-by":"publisher","DOI":"10.1071\/CP19016"},{"key":"e_1_2_7_59_1","doi-asserted-by":"publisher","DOI":"10.3390\/f6103686"},{"key":"e_1_2_7_60_1","doi-asserted-by":"publisher","DOI":"10.3390\/proteomes5040029"},{"key":"e_1_2_7_61_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2019.00046"},{"key":"e_1_2_7_62_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00344-013-9402-0"},{"key":"e_1_2_7_63_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.1985.tb02784.x"},{"key":"e_1_2_7_64_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2019.02.023"},{"issue":"34","key":"e_1_2_7_65_1","first-page":"97","article-title":"Nitrogen in agriculture: Balancing the cost of an essential resource","volume":"34","author":"Robertson G. P.","year":"2009","journal-title":"Social Science Electronic Publishing"},{"key":"e_1_2_7_66_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40502-013-0049-4"},{"key":"e_1_2_7_67_1","first-page":"303","article-title":"Effect of rhizobium inoculation to nodulation and growth of soybean (Glycine max (L.) Merrill) germplasm","volume":"41","author":"Samudin S.","year":"2018","journal-title":"Legume Research"},{"key":"e_1_2_7_68_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2009.03890.x"},{"key":"e_1_2_7_69_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.77.3.779"},{"key":"e_1_2_7_70_1","doi-asserted-by":"publisher","DOI":"10.2135\/cropsci1989.0011183X002900010023x"},{"key":"e_1_2_7_71_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2013.11.003"},{"key":"e_1_2_7_72_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.124.2.531"},{"key":"e_1_2_7_73_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erv030"},{"key":"e_1_2_7_74_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11738-016-2163-1"},{"key":"e_1_2_7_75_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.110.156430"},{"key":"e_1_2_7_76_1","doi-asserted-by":"publisher","DOI":"10.1021\/pr300465n"},{"key":"e_1_2_7_77_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10535-017-0722-y"},{"key":"e_1_2_7_78_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11104-014-2166-x"},{"key":"e_1_2_7_79_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-02872-0"},{"key":"e_1_2_7_80_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.62.3.443"},{"key":"e_1_2_7_81_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41438-018-0029-y"},{"key":"e_1_2_7_82_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.13898"},{"key":"e_1_2_7_83_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12155-014-9566-x"},{"key":"e_1_2_7_84_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10535-012-0116-0"},{"issue":"12","key":"e_1_2_7_85_1","first-page":"1402","article-title":"Study of nitrogen pollution in Croatia by moss biomonitoring and Kjeldahl method","volume":"49","author":"Zdravko S.","year":"2014","journal-title":"Environmental Letters"},{"key":"e_1_2_7_86_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00438-016-1275-z"},{"key":"e_1_2_7_87_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11738-010-0469-y"},{"key":"e_1_2_7_88_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00344-015-9498-5"},{"key":"e_1_2_7_89_1","doi-asserted-by":"publisher","DOI":"10.21273\/HORTSCI.51.2.152"},{"key":"e_1_2_7_90_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-018-5342-1"},{"key":"e_1_2_7_91_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.01288"},{"key":"e_1_2_7_92_1","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-01-19-0003-R"}],"container-title":["Plant, Cell &amp; Environment"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fpce.13736","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pce.13736","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/pce.13736","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pce.13736","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,5]],"date-time":"2023-09-05T16:36:57Z","timestamp":1693931817000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/pce.13736"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,18]]},"references-count":91,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2020,5]]}},"alternative-id":["10.1111\/pce.13736"],"URL":"https:\/\/doi.org\/10.1111\/pce.13736","archive":["Portico"],"relation":{},"ISSN":["0140-7791","1365-3040"],"issn-type":[{"value":"0140-7791","type":"print"},{"value":"1365-3040","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,18]]},"assertion":[{"value":"2019-05-21","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-01-26","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-02-18","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}