{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T14:47:26Z","timestamp":1785422846691,"version":"3.56.0"},"reference-count":39,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T00:00:00Z","timestamp":1781481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key R&D Program of China","doi-asserted-by":"crossref","award":["2024YFA0918200"],"award-info":[{"award-number":["2024YFA0918200"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100012166","name":"National Key R&D Program of China","doi-asserted-by":"crossref","award":["2019YFA0904700"],"award-info":[{"award-number":["2019YFA0904700"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32270254"],"award-info":[{"award-number":["32270254"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32470102"],"award-info":[{"award-number":["32470102"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["31970266"],"award-info":[{"award-number":["31970266"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["31770096"],"award-info":[{"award-number":["31770096"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"award":["32270254"],"award-info":[{"award-number":["32270254"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"award":["32470102"],"award-info":[{"award-number":["32470102"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"award":["31970266"],"award-info":[{"award-number":["31970266"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"award":["31770096"],"award-info":[{"award-number":["31770096"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Suzhou Science and Technology Bureau","award":["SZKJXM202502"],"award-info":[{"award-number":["SZKJXM202502"]}]},{"award":["SZKJXM202502"],"award-info":[{"award-number":["SZKJXM202502"]}],"id":[{"id":"https:\/\/ror.org\/02vpk4745","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Agricultural Technology Innovation Project of Jurong","award":["ZA32417"],"award-info":[{"award-number":["ZA32417"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antioxidants"],"abstract":"<jats:p>Many rhizobia use quorum sensing (QS) systems to detect their population density and modify their symbiotic behavior with the legume host. There are three LuxRI-type QS systems in Rhizobium etli CFN42, and CinR plays a key role in symbiotic performance. However, the details of how CinR regulates the symbiotic process remain unknown. In this study, we employed the RNA-Seq method to screen differentially expressed genes between the wild-type strain and the \u0394cinR mutant of R. etli CFN42. We found that most of the genes related to reactive oxygen species (ROS) were expressed at lower levels in the \u0394cinR mutant than in CFN42. We also found that the \u0394cinR mutant was more sensitive to H2O2 than to CFN42. We then showed that CinR positively regulated katG expression and possessed an affinity to bind the katG promoter in the absence of the AHL ligand. The addition of AHLs promoted CinR binding to the katG promoter and enhanced katG expression. Accumulation of H2O2 and O2\u2022\u2212 was observed in root nodules formed by the \u0394cinR mutant. Crucially, katG overexpression rescued the H2O2-sensitive phenotype in vitro and partially restored defective symbiotic performance in nodules formed by the \u0394cinR mutant on the common bean. These results suggest that CinR globally regulates ROS scavenging gene expression in order to balance oxidative stress within root nodules, promoting nitrogenase activity of R. etli CFN42.<\/jats:p>","DOI":"10.3390\/antiox15060752","type":"journal-article","created":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T08:22:56Z","timestamp":1781684576000},"page":"752","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Quorum Sensing Regulator CinR Directly Activates the Catalase\u2013Peroxidase Gene katG to Alleviate Oxidative Stress and Promote Symbiotic Nitrogen Fixation in Rhizobium etli CFN42"],"prefix":"10.3390","volume":"15","author":[{"given":"Xuelian","family":"Chen","sequence":"first","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianyi","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhi","family":"Zheng","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chuling","family":"Gan","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Lin","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Siqing","family":"Yin","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zi","family":"Li","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongjian","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-3675-8801","authenticated-orcid":false,"given":"Yajun","family":"Cao","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9845-8594","authenticated-orcid":false,"given":"Zhi","family":"Huang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8865-3599","authenticated-orcid":false,"given":"Hui","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guoxi","family":"Zhang","sequence":"additional","affiliation":[{"name":"Nanjing Yuanjian Bioengineering Co., Ltd., Nanjing 210046, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0223-8875","authenticated-orcid":false,"given":"Zengtao","family":"Zhong","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,6,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1093\/aob\/mct048","article-title":"Biological nitrogen fixation in non-legume plants","volume":"111","author":"Santi","year":"2013","journal-title":"Ann. Bot."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1128\/MMBR.67.4.574-592.2003","article-title":"Quorum sensing in nitrogen-fixing rhizobia","volume":"67","author":"Gonzalez","year":"2003","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1098\/rstb.2007.2041","article-title":"Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes","volume":"362","author":"Bauer","year":"2007","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Calatrava-Morales, N., McIntosh, M., and Soto, M. (2018). Regulation mediated by N-acyl homoserine lactone quorum sensing signals in the rhizobium-legume symbiosis. Genes, 9.","DOI":"10.3390\/genes9050263"},{"key":"ref_5","first-page":"4104","article-title":"Ribosomal frameshifting and dual-target antiactivation restrict quorum-sensing-activated transfer of a mobile genetic element","volume":"112","author":"Ramsay","year":"2015","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1943","DOI":"10.1128\/JB.188.5.1943-1949.2006","article-title":"A LuxR\/LuxI-type quorum-sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation","volume":"188","author":"Zheng","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Taboada-Castro, H., Gil, J., Gomez-Caudillo, L., Escorcia-Rodriguez, J.M., Freyre-Gonzalez, J.A., and Encarnacion-Guevara, S. (2022). Rhizobium etli CFN42 proteomes showed isoenzymes in free-living and symbiosis with a different transcriptional regulation inferred from a transcriptional regulatory network. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.947678"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1573","DOI":"10.1128\/JB.00003-15","article-title":"The quorum sensing regulator CinR hierarchically regulates two other quorum sensing pathways in ligand-dependent and -independent fashions in Rhizobium etli","volume":"197","author":"Zheng","year":"2015","journal-title":"J. Bacteriol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1038\/ismej.2008.13","article-title":"AHL-driven quorum-sensing circuits: Their frequency and function among the Proteobacteria","volume":"2","author":"Case","year":"2008","journal-title":"ISME J."},{"key":"ref_10","first-page":"1314","article-title":"Effectiveness of nitrogen fixation in rhizobia","volume":"13","author":"Mousavi","year":"2019","journal-title":"Microb. Biotechnol."},{"key":"ref_11","first-page":"109","article-title":"Leghemoglobins and leghemoglobin genes","volume":"35","author":"Konieczny","year":"1989","journal-title":"Postep. Biochem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2202","DOI":"10.1089\/ars.2012.5136","article-title":"Hydrogen peroxide and nitric oxide: Key regulators of the legume\u2014Rhizobium and mycorrhizal symbioses","volume":"18","author":"Puppo","year":"2013","journal-title":"Antioxid. Redox Signal."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1111\/nph.18434","article-title":"Signaling by reactive molecules and antioxidants in legume nodules","volume":"236","author":"Matamoros","year":"2022","journal-title":"New Phytol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e0053920","DOI":"10.1128\/JB.00539-20","article-title":"How rhizobia adapt to the nodule environment","volume":"203","author":"Ledermann","year":"2021","journal-title":"J. Bacteriol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Mandon, K., Nazaret, F., Farajzadeh, D., Alloing, G., and Frendo, P. (2021). Redox regulation in diazotrophic bacteria in interaction with plants. Antioxidants, 10.","DOI":"10.3390\/antiox10060880"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"fnw130","DOI":"10.1093\/femsle\/fnw130","article-title":"OxyR-regulated catalase activity is critical for oxidative stress resistance, nodulation and nitrogen fixation in Azorhizobium caulinodans","volume":"363","author":"Zhao","year":"2016","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1007\/s00203-019-01654-8","article-title":"Bacterioferritin comigratory protein is important in hydrogen peroxide resistance, nodulation, and nitrogen fixation in Azorhizobium caulinodans","volume":"201","author":"Liu","year":"2019","journal-title":"Arch. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1128\/jb.158.1.148-155.1984","article-title":"Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions","volume":"158","author":"Noel","year":"1984","journal-title":"J. Bacteriol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"6949","DOI":"10.1128\/AEM.69.11.6949-6953.2003","article-title":"Agrobacterium bioassay strain for ultrasensitive detection of N-Acylhomoserine lactone-type quorum-sensing molecules: Detection of autoinducers in Mesorhizobium huakuii","volume":"69","author":"Zhu","year":"2003","journal-title":"Appl. Envion. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1007\/s00203-007-0345-3","article-title":"Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: Plant host interaction","volume":"189","author":"Wang","year":"2008","journal-title":"Arch. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"15773","DOI":"10.1074\/jbc.M200109200","article-title":"Mutations in the occQ operator that decrease OccR-induced DNA bending do not cause constitutive promoter activity","volume":"277","author":"Akakura","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1101\/gr.086595.108","article-title":"Dissecting transcription regulatory pathways through a new bacterial one-hybrid reporter system","volume":"19","author":"Guo","year":"2009","journal-title":"Genome Res."},{"key":"ref_23","first-page":"374","article-title":"The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique","volume":"16","author":"Fahraeus","year":"1957","journal-title":"J. Gen. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"13875","DOI":"10.1073\/pnas.1615121113","article-title":"Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island","volume":"113","author":"Ling","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1139\/x82-098","article-title":"Nitrogen fixation and acetylene reduction in decaying conifer boles: Effects of incubation time, aeration, and moisture content","volume":"12","author":"Silvester","year":"1982","journal-title":"Can. J. For. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1146\/annurev.pp.44.060193.002411","article-title":"Gas exchange of legume nodules and the regulation of nitrogenase activity","volume":"44","author":"Hunt","year":"2003","journal-title":"Annu. Rev. Plant Physiol. Plant Mol. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1118","DOI":"10.1093\/oxfordjournals.pcp.a029096","article-title":"Generation of auperoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: Their association with lignification","volume":"38","author":"Sumio","year":"1997","journal-title":"Plant Cell Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1104\/pp.114.238873","article-title":"The emerging role of reactive oxygen species signaling during lateral root development","volume":"165","author":"Manzano","year":"2014","journal-title":"Plant Physiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1099\/mic.0.25909-0","article-title":"Only one catalase, katG, is detectable in Rhizobium etli, and is encoded along with the regulator OxyR on a plasmid replicon","volume":"149","author":"Mora","year":"2003","journal-title":"Microbiology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.abb.2012.04.014","article-title":"Why do bacteria use so many enzymes to scavenge hydrogen peroxide?","volume":"525","author":"Mishra","year":"2012","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1038\/nrmicro954","article-title":"Genetic regulation of biological nitrogen fixation","volume":"2","author":"Dixon","year":"2004","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Satchell, K.J.F., Wang, H., Xing, X., Wang, J., Pang, B., Liu, M., Larios-Valencia, J., Liu, T., Liu, G., and Xie, S. (2018). Hypermutation-induced in vivo oxidative stress resistance enhances Vibrio cholerae host adaptation. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1007413"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"fnz014","DOI":"10.1093\/femsle\/fnz014","article-title":"Alkyl hydroperoxide reductase is important for oxidative stress resistance and symbiosis in Azorhizobium caulinodans","volume":"366","author":"Jiang","year":"2019","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Orihuela, C.J., Niu, K., Meng, Y., Liu, M., Ma, Z., Lin, H., Zhou, H., and Fan, H. (2023). Phosphorylation of GntR reduces Streptococcus suis oxidative stress resistance and virulence by inhibiting NADH oxidase transcription. PLoS Pathog., 19.","DOI":"10.1371\/journal.ppat.1011227"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1128\/JB.185.5.1681-1692.2003","article-title":"Conjugative transfer of p42a from Rhizobium etli CFN42, which is required for mobilization of the symbiotic plasmid, is regulated by quorum sensing","volume":"185","author":"Bustos","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1007\/s00203-018-1478-2","article-title":"Soil commensal rhizobia promote Rhizobium etli nodulation efficiency through CinR-mediated quorum sensing","volume":"200","author":"Miao","year":"2018","journal-title":"Arch. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/j.1469-8137.1992.tb04227.x","article-title":"Developmental biology of legume nodulation","volume":"122","author":"Hirsch","year":"1992","journal-title":"New Phytol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"105426","DOI":"10.1016\/j.rvsc.2024.105426","article-title":"Oxidative stress response in avian pathogenic Escherichia coli","volume":"180","author":"Yu","year":"2024","journal-title":"Res. Vet. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Kim, J.H., Dong, J., Le, B.H., Lonergan, Z.R., Gu, W., Girke, T., Zhang, W., Newman, D.K., and Martins-Green, M. (2024). Pseudomonas aeruginosa activates quorum sensing, antioxidant enzymes and type vi secretion in response to oxidative stress to initiate biofilm formation and wound chronicity. Antioxidants, 13.","DOI":"10.3390\/antiox13060655"}],"container-title":["Antioxidants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3921\/15\/6\/752\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T04:31:12Z","timestamp":1781843472000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3921\/15\/6\/752"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,15]]},"references-count":39,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6]]}},"alternative-id":["antiox15060752"],"URL":"https:\/\/doi.org\/10.3390\/antiox15060752","relation":{},"ISSN":["2076-3921"],"issn-type":[{"value":"2076-3921","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,15]]}}}