{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T19:25:39Z","timestamp":1790364339819,"version":"4.1.0"},"reference-count":54,"publisher":"American Society for Microbiology","issue":"14","license":[{"start":{"date-parts":[[2018,7,15]],"date-time":"2018-07-15T00:00:00Z","timestamp":1531612800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Appl Environ Microbiol"],"published-print":{"date-parts":[[2018,7,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    This study determined the function of thioredoxin and glutaredoxin systems in the phytopathogenic fungus\n                    <jats:named-content content-type=\"genus-species\">Alternaria alternata<\/jats:named-content>\n                    via analyzing mutants obtained from the targeted deletion of genes encoding thioredoxin peroxidase (\n                    <jats:italic>Tsa1<\/jats:italic>\n                    ), thioredoxin reductase (\n                    <jats:italic>Trr1<\/jats:italic>\n                    ), and glutathione reductase (\n                    <jats:italic>Glr1<\/jats:italic>\n                    ).\n                    <jats:italic>Trr1<\/jats:italic>\n                    and\n                    <jats:italic>Glr1<\/jats:italic>\n                    , but not\n                    <jats:italic>Tsa1<\/jats:italic>\n                    , are required for growth and conidiation. The reduced growth and conidiation seen in the\n                    <jats:italic>Trr1<\/jats:italic>\n                    or\n                    <jats:italic>Glr1<\/jats:italic>\n                    deletion mutant can be restored by glutathione. Deletion mutants showing growth inhibition by oxidants are defective for H\n                    <jats:sub>2<\/jats:sub>\n                    O\n                    <jats:sub>2<\/jats:sub>\n                    detoxification and induce smaller lesions on citrus leaves.\n                    <jats:italic>Trr1<\/jats:italic>\n                    and\n                    <jats:italic>Glr1<\/jats:italic>\n                    , but not\n                    <jats:italic>Tsa1<\/jats:italic>\n                    , also contribute to NaCl resistance.\n                    <jats:italic>Glr1<\/jats:italic>\n                    is required for sorbitol resistance and is responsible for resistance to mancozeb and boscalid but not chlorothalonil fungicides, a novel phenotype that has not been reported in fungi.\n                    <jats:italic>Trr1<\/jats:italic>\n                    is required for resistance to boscalid and chlorothalonil fungicides but confers susceptibility to mancozeb. The\n                    <jats:italic>Tsa1<\/jats:italic>\n                    deletion mutant displays wild-type sensitivity to the tested fungicides. The expression of\n                    <jats:italic>Tsa1<\/jats:italic>\n                    and\n                    <jats:italic>Trr1<\/jats:italic>\n                    is regulated by the oxidative stress responsive regulators Yap1, Hog1, and Skn7. The expression of\n                    <jats:italic>Tsa1<\/jats:italic>\n                    , but not\n                    <jats:italic>Trr1<\/jats:italic>\n                    , is also regulated indirectly by the NADPH oxidase. The results indicate that the capability to resist oxidative stress is required for virulence of\n                    <jats:named-content content-type=\"genus-species\">A. alternata<\/jats:named-content>\n                    .\n                  <\/jats:p>\n                  <jats:p>\n                    <jats:bold>IMPORTANCE<\/jats:bold>\n                    The thioredoxin and glutaredoxin systems are important thiol antioxidant systems in cells, and knowledge of these two systems in the plant-pathogenic fungus\n                    <jats:named-content content-type=\"genus-species\">A. alternata<\/jats:named-content>\n                    is useful for finding new strategies to reduce the virulence of this pathogen. In this study, we demonstrated that thiol antioxidant system-related genes (\n                    <jats:italic>Tsa1<\/jats:italic>\n                    ,\n                    <jats:italic>Trr1<\/jats:italic>\n                    , and\n                    <jats:italic>Glr1<\/jats:italic>\n                    ) are required for H\n                    <jats:sub>2<\/jats:sub>\n                    O\n                    <jats:sub>2<\/jats:sub>\n                    detoxification and virulence in\n                    <jats:named-content content-type=\"genus-species\">A. alternata<\/jats:named-content>\n                    . Moreover, deletion of\n                    <jats:italic>Trr1<\/jats:italic>\n                    results in hypersensitivity to the fungicides chlorothalonil and boscalid, and\n                    <jats:italic>Glr1<\/jats:italic>\n                    deletion mutants are highly sensitive to mancozeb, which is the fungicide mostly used in citrus fields. Therefore, our findings demonstrate that the ability to detoxify reactive oxygen species (ROS) plays a critical role in pathogenesis on citrus and provide novel insights into the physiological functions of thiol-containing systems in fungicide sensitivity for\n                    <jats:named-content content-type=\"genus-species\">A. alternata<\/jats:named-content>\n                    .\n                  <\/jats:p>","DOI":"10.1128\/aem.00086-18","type":"journal-article","created":{"date-parts":[[2018,5,9]],"date-time":"2018-05-09T05:19:04Z","timestamp":1525843144000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":63,"title":["Thioredoxin and Glutaredoxin Systems Required for Oxidative Stress Resistance, Fungicide Sensitivity, and Virulence of Alternaria alternata"],"prefix":"10.1128","volume":"84","author":[{"given":"Haijie","family":"Ma","sequence":"first","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mingshuang","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunpeng","family":"Gai","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huilan","family":"Fu","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bin","family":"Zhang","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruoxin","family":"Ruan","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kuang-Ren","family":"Chung","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology, College of Agriculture and Natural Resources, National Chung-Hsing University, Taichung, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongye","family":"Li","sequence":"additional","affiliation":[{"name":"Institute of Biotechnology, Zhejiang University, Hangzhou, China"},{"name":"Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-phyto-072910-095355"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1001335"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1111\/nph.12530"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1042\/BST0331375"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1093\/aob\/mcf118"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)71625-6"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2001.02283.x"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2004.05.002"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2004.03921.x"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1000524"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2011.07.027"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-01-14-0012-R"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1128\/EC.00083-07"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.00313-10"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.28132-0"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0087300"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12484"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1094\/Phyto-81-719"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00284-010-9795-y"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.freeradbiomed.2017.11.028"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.pmpp.2014.08.001"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-22-8-0942"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2010.06.009"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2012.07.006"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12026"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.13125"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1038\/srep32437"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.micro.54.1.439"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0968-0004(02)00003-8"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2035018100"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2017.11.011"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.275.8.5723"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/0048-3575(73)90100-4"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10658-008-9290-5"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1007\/s001289901020"},{"key":"e_1_3_3_37_2","first-page":"155","article-title":"Mode of action of carboximides","volume":"9","author":"Kuhn PJ","year":"1984","unstructured":"Kuhn PJ. 1984. Mode of action of carboximides. Br Mycol Soc Sym Ser 9:155\u2013183.","journal-title":"Br Mycol Soc Sym Ser"},{"key":"e_1_3_3_38_2","first-page":"287","article-title":"Effects of boscalid on the antioxidant enzyme system of adult zebrafish (Danio rerio)","volume":"18","author":"Zang X","year":"2017","unstructured":"Zang X, Wang M, Zhang XY, Tian XH. 2017. Effects of boscalid on the antioxidant enzyme system of adult zebrafish (Danio rerio). Agric Sci Technol 18:287\u2013293.","journal-title":"Agric Sci Technol"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/B978-012426260-7.50082-3"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1091\/mbc.7.11.1805"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11274-017-2325-3"},{"key":"e_1_3_3_42_2","volume-title":"Pesticide toxicology and international regulation","author":"Marrs TT","year":"2004","unstructured":"Marrs TT, Ballantyne B (ed). 2004. Pesticide toxicology and international regulation. John Wiley & Sons, New York, NY."},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuro.2007.04.008"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.1089\/omi.2009.0134"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.redox.2014.04.007"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbrc.2007.12.056"},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.3390\/biom5010142"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2014.10.015"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1364-3703.2012.00799.x"},{"key":"e_1_3_3_50_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6968.2002.tb11282.x"},{"key":"e_1_3_3_51_2","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/978-3-319-10503-1_15","volume-title":"Genetic transformation systems in fungi","author":"Chung KR","year":"2015","unstructured":"Chung KR, Lee MH. 2015. Split-marker-mediated transformation and targeted gene disruption in filamentous fungi, p 175\u2013180. In van den Berg M, Maruthachalam K (ed), Genetic transformation systems in fungi, vol 2. Springer International Publishing, Cham, Switzerland."},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1631\/jzus.B0860006"},{"key":"e_1_3_3_53_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00253-011-3355-7"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1472-765X.1985.tb01479.x"},{"key":"e_1_3_3_55_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2009.12.009"}],"container-title":["Applied and Environmental Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/AEM.00086-18","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/AEM.00086-18","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,23]],"date-time":"2022-02-23T13:43:56Z","timestamp":1645623836000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/AEM.00086-18"}},"subtitle":[],"editor":[{"given":"Emma R.","family":"Master","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,7,15]]},"references-count":54,"journal-issue":{"issue":"14","published-print":{"date-parts":[[2018,7,15]]}},"alternative-id":["10.1128\/AEM.00086-18"],"URL":"https:\/\/doi.org\/10.1128\/aem.00086-18","relation":{},"ISSN":["0099-2240","1098-5336"],"issn-type":[{"value":"0099-2240","type":"print"},{"value":"1098-5336","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,7,15]]},"assertion":[{"value":"2018-01-12","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-05-04","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-07-02","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00086-18"}}