Translocon Subunits of the COP9 Signalosome Complex Are a Central Hub for Regulating Multiple Photoresponsive Processes and Autophagic Flux in Magnaporthe oryzae
Photodependent processes, including circadian rhythm, autophagy, ubiquitination, neddylation/deneddylation, and metabolite biosynthesis, profoundly influence microbial pathogenesis. Although a photomorphogenesis signalosome (COP9/CSN) has been identified, the mechanism by which this large complex co...
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| Veröffentlicht in: | Journal of agricultural and food chemistry 2024-10, Vol.72 (40), p.22015-22034 |
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| creator | Lin, Lili Guo, Hengyuan Batool, Wajjiha Lin, Lianyu Cao, Jiaying An, Qiuli Aliyu, Sami Rukaiya Bao, Jiandong Wang, Zonghua Norvienyeku, Justice |
| description | Photodependent processes, including circadian rhythm, autophagy, ubiquitination, neddylation/deneddylation, and metabolite biosynthesis, profoundly influence microbial pathogenesis. Although a photomorphogenesis signalosome (COP9/CSN) has been identified, the mechanism by which this large complex contributes to the pathophysiological processes in filamentous fungi remains unclear. Here, we identified eight CSN complex subunits in the rice blast fungus Magnaporthe oryzae and functionally characterized the translocon subunits containing a nuclear export or localization signal (NES/NLS). Targeted gene replacement of these CSN subunits, including MoCSN3, MoCSN5, MoCSN6, MoCSN7, and MoCSN12, attenuated vegetative growth and conidiation and rendered the deletion strains nonpathogenic. MoCSN7 deletion significantly suppressed arachidonic acid catabolism, and compromised cell wall integrity in M. oryzae. Surprisingly, we also discovered that MoCSN subunits, particularly MoCsn7, are required for the cAMP-dependent regulation of autophagic flux. Therefore, MoCSN significantly contributes to morphological, physiological, and pathogenic differentiation in M. oryzae by fostering cross-talk between multiple pathways. |
| doi_str_mv | 10.1021/acs.jafc.4c03163 |
| format | Article |
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Although a photomorphogenesis signalosome (COP9/CSN) has been identified, the mechanism by which this large complex contributes to the pathophysiological processes in filamentous fungi remains unclear. Here, we identified eight CSN complex subunits in the rice blast fungus Magnaporthe oryzae and functionally characterized the translocon subunits containing a nuclear export or localization signal (NES/NLS). Targeted gene replacement of these CSN subunits, including MoCSN3, MoCSN5, MoCSN6, MoCSN7, and MoCSN12, attenuated vegetative growth and conidiation and rendered the deletion strains nonpathogenic. MoCSN7 deletion significantly suppressed arachidonic acid catabolism, and compromised cell wall integrity in M. oryzae. Surprisingly, we also discovered that MoCSN subunits, particularly MoCsn7, are required for the cAMP-dependent regulation of autophagic flux. Therefore, MoCSN significantly contributes to morphological, physiological, and pathogenic differentiation in M. oryzae by fostering cross-talk between multiple pathways.</description><identifier>ISSN: 0021-8561</identifier><identifier>ISSN: 1520-5118</identifier><identifier>EISSN: 1520-5118</identifier><identifier>DOI: 10.1021/acs.jafc.4c03163</identifier><identifier>PMID: 39319468</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Agricultural and Environmental Chemistry ; arachidonic acid ; Ascomycota - genetics ; Ascomycota - metabolism ; Autophagy ; biosynthesis ; blast disease ; catabolism ; cell walls ; circadian rhythm ; conidiation ; constitutive photomorphogenesis 9 signalosome ; COP9 Signalosome Complex - genetics ; COP9 Signalosome Complex - metabolism ; food chemistry ; Fungal Proteins - genetics ; Fungal Proteins - metabolism ; fungi ; Gene Expression Regulation, Fungal ; genes ; Light ; Magnaporthe oryzae ; metabolites ; Oryza - genetics ; Oryza - metabolism ; Oryza - microbiology ; pathogenesis ; photomorphogenesis ; physiological transport ; Plant Diseases - microbiology ; ubiquitination ; vegetative growth</subject><ispartof>Journal of agricultural and food chemistry, 2024-10, Vol.72 (40), p.22015-22034</ispartof><rights>2024 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a252t-ac4f71d7de49dc3a4f04a6258cdf0a632d7f1f2b8cec648a3d3320af8a82ae8d3</cites><orcidid>0000-0002-8322-5293</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.jafc.4c03163$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.jafc.4c03163$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39319468$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lin, Lili</creatorcontrib><creatorcontrib>Guo, Hengyuan</creatorcontrib><creatorcontrib>Batool, Wajjiha</creatorcontrib><creatorcontrib>Lin, Lianyu</creatorcontrib><creatorcontrib>Cao, Jiaying</creatorcontrib><creatorcontrib>An, Qiuli</creatorcontrib><creatorcontrib>Aliyu, Sami Rukaiya</creatorcontrib><creatorcontrib>Bao, Jiandong</creatorcontrib><creatorcontrib>Wang, Zonghua</creatorcontrib><creatorcontrib>Norvienyeku, Justice</creatorcontrib><title>Translocon Subunits of the COP9 Signalosome Complex Are a Central Hub for Regulating Multiple Photoresponsive Processes and Autophagic Flux in Magnaporthe oryzae</title><title>Journal of agricultural and food chemistry</title><addtitle>J. Agric. Food Chem</addtitle><description>Photodependent processes, including circadian rhythm, autophagy, ubiquitination, neddylation/deneddylation, and metabolite biosynthesis, profoundly influence microbial pathogenesis. Although a photomorphogenesis signalosome (COP9/CSN) has been identified, the mechanism by which this large complex contributes to the pathophysiological processes in filamentous fungi remains unclear. Here, we identified eight CSN complex subunits in the rice blast fungus Magnaporthe oryzae and functionally characterized the translocon subunits containing a nuclear export or localization signal (NES/NLS). Targeted gene replacement of these CSN subunits, including MoCSN3, MoCSN5, MoCSN6, MoCSN7, and MoCSN12, attenuated vegetative growth and conidiation and rendered the deletion strains nonpathogenic. MoCSN7 deletion significantly suppressed arachidonic acid catabolism, and compromised cell wall integrity in M. oryzae. Surprisingly, we also discovered that MoCSN subunits, particularly MoCsn7, are required for the cAMP-dependent regulation of autophagic flux. Therefore, MoCSN significantly contributes to morphological, physiological, and pathogenic differentiation in M. oryzae by fostering cross-talk between multiple pathways.</description><subject>Agricultural and Environmental Chemistry</subject><subject>arachidonic acid</subject><subject>Ascomycota - genetics</subject><subject>Ascomycota - metabolism</subject><subject>Autophagy</subject><subject>biosynthesis</subject><subject>blast disease</subject><subject>catabolism</subject><subject>cell walls</subject><subject>circadian rhythm</subject><subject>conidiation</subject><subject>constitutive photomorphogenesis 9 signalosome</subject><subject>COP9 Signalosome Complex - genetics</subject><subject>COP9 Signalosome Complex - metabolism</subject><subject>food chemistry</subject><subject>Fungal Proteins - genetics</subject><subject>Fungal Proteins - metabolism</subject><subject>fungi</subject><subject>Gene Expression Regulation, Fungal</subject><subject>genes</subject><subject>Light</subject><subject>Magnaporthe oryzae</subject><subject>metabolites</subject><subject>Oryza - genetics</subject><subject>Oryza - metabolism</subject><subject>Oryza - microbiology</subject><subject>pathogenesis</subject><subject>photomorphogenesis</subject><subject>physiological transport</subject><subject>Plant Diseases - microbiology</subject><subject>ubiquitination</subject><subject>vegetative growth</subject><issn>0021-8561</issn><issn>1520-5118</issn><issn>1520-5118</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtvEzEURi0EoqGwZ4W8ZMEEP-bhWUZRS5FataJlPbrxI5nKYw9-oJZ_039ahwR2SKyu7tX5vrs4CL2nZEkJo59BxuU9GLmsJeG05S_QgjaMVA2l4iVakMJUomnpCXoT4z0hRDQdeY1OeM9pX7digZ7uArhovfQO3-ZNdmOK2Bucdhqvr296fDtuHVgf_VQOfpqtfsCroDHgtXYpgMUXeYOND_ib3mYLaXRbfJVtGguKb3Y--aDj7F0cf5Y9eKlj1BGDU3iVk593sB0lPrf5AY8OX0F5N_uw_-_D4y_Qb9ErAzbqd8d5ir6fn92tL6rL6y9f16vLCljDUgWyNh1VndJ1rySH2pAaWtYIqQyBljPVGWrYRkgt21oAV5wzAkaAYKCF4qfo46F3Dv5H1jEN0xilthac9jkOnDZc8IYQ_h8o6WvWd3VTUHJAZfAxBm2GOYwThMeBkmHvcCgOh73D4eiwRD4c2_Nm0upv4I-0Anw6AL-jPociKP677xltvas9</recordid><startdate>20241009</startdate><enddate>20241009</enddate><creator>Lin, Lili</creator><creator>Guo, Hengyuan</creator><creator>Batool, Wajjiha</creator><creator>Lin, Lianyu</creator><creator>Cao, Jiaying</creator><creator>An, Qiuli</creator><creator>Aliyu, Sami Rukaiya</creator><creator>Bao, Jiandong</creator><creator>Wang, Zonghua</creator><creator>Norvienyeku, Justice</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-8322-5293</orcidid></search><sort><creationdate>20241009</creationdate><title>Translocon Subunits of the COP9 Signalosome Complex Are a Central Hub for Regulating Multiple Photoresponsive Processes and Autophagic Flux in Magnaporthe oryzae</title><author>Lin, Lili ; Guo, Hengyuan ; Batool, Wajjiha ; Lin, Lianyu ; Cao, Jiaying ; An, Qiuli ; Aliyu, Sami Rukaiya ; Bao, Jiandong ; Wang, Zonghua ; Norvienyeku, Justice</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a252t-ac4f71d7de49dc3a4f04a6258cdf0a632d7f1f2b8cec648a3d3320af8a82ae8d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Agricultural and Environmental Chemistry</topic><topic>arachidonic acid</topic><topic>Ascomycota - genetics</topic><topic>Ascomycota - metabolism</topic><topic>Autophagy</topic><topic>biosynthesis</topic><topic>blast disease</topic><topic>catabolism</topic><topic>cell walls</topic><topic>circadian rhythm</topic><topic>conidiation</topic><topic>constitutive photomorphogenesis 9 signalosome</topic><topic>COP9 Signalosome Complex - genetics</topic><topic>COP9 Signalosome Complex - metabolism</topic><topic>food chemistry</topic><topic>Fungal Proteins - genetics</topic><topic>Fungal Proteins - metabolism</topic><topic>fungi</topic><topic>Gene Expression Regulation, Fungal</topic><topic>genes</topic><topic>Light</topic><topic>Magnaporthe oryzae</topic><topic>metabolites</topic><topic>Oryza - genetics</topic><topic>Oryza - metabolism</topic><topic>Oryza - microbiology</topic><topic>pathogenesis</topic><topic>photomorphogenesis</topic><topic>physiological transport</topic><topic>Plant Diseases - microbiology</topic><topic>ubiquitination</topic><topic>vegetative growth</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lin, Lili</creatorcontrib><creatorcontrib>Guo, Hengyuan</creatorcontrib><creatorcontrib>Batool, Wajjiha</creatorcontrib><creatorcontrib>Lin, Lianyu</creatorcontrib><creatorcontrib>Cao, Jiaying</creatorcontrib><creatorcontrib>An, Qiuli</creatorcontrib><creatorcontrib>Aliyu, Sami Rukaiya</creatorcontrib><creatorcontrib>Bao, Jiandong</creatorcontrib><creatorcontrib>Wang, Zonghua</creatorcontrib><creatorcontrib>Norvienyeku, Justice</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Journal of agricultural and food chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lin, Lili</au><au>Guo, Hengyuan</au><au>Batool, Wajjiha</au><au>Lin, Lianyu</au><au>Cao, Jiaying</au><au>An, Qiuli</au><au>Aliyu, Sami Rukaiya</au><au>Bao, Jiandong</au><au>Wang, Zonghua</au><au>Norvienyeku, Justice</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Translocon Subunits of the COP9 Signalosome Complex Are a Central Hub for Regulating Multiple Photoresponsive Processes and Autophagic Flux in Magnaporthe oryzae</atitle><jtitle>Journal of agricultural and food chemistry</jtitle><addtitle>J. Agric. Food Chem</addtitle><date>2024-10-09</date><risdate>2024</risdate><volume>72</volume><issue>40</issue><spage>22015</spage><epage>22034</epage><pages>22015-22034</pages><issn>0021-8561</issn><issn>1520-5118</issn><eissn>1520-5118</eissn><abstract>Photodependent processes, including circadian rhythm, autophagy, ubiquitination, neddylation/deneddylation, and metabolite biosynthesis, profoundly influence microbial pathogenesis. Although a photomorphogenesis signalosome (COP9/CSN) has been identified, the mechanism by which this large complex contributes to the pathophysiological processes in filamentous fungi remains unclear. Here, we identified eight CSN complex subunits in the rice blast fungus Magnaporthe oryzae and functionally characterized the translocon subunits containing a nuclear export or localization signal (NES/NLS). Targeted gene replacement of these CSN subunits, including MoCSN3, MoCSN5, MoCSN6, MoCSN7, and MoCSN12, attenuated vegetative growth and conidiation and rendered the deletion strains nonpathogenic. MoCSN7 deletion significantly suppressed arachidonic acid catabolism, and compromised cell wall integrity in M. oryzae. Surprisingly, we also discovered that MoCSN subunits, particularly MoCsn7, are required for the cAMP-dependent regulation of autophagic flux. Therefore, MoCSN significantly contributes to morphological, physiological, and pathogenic differentiation in M. oryzae by fostering cross-talk between multiple pathways.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>39319468</pmid><doi>10.1021/acs.jafc.4c03163</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-8322-5293</orcidid></addata></record> |
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| subjects | Agricultural and Environmental Chemistry arachidonic acid Ascomycota - genetics Ascomycota - metabolism Autophagy biosynthesis blast disease catabolism cell walls circadian rhythm conidiation constitutive photomorphogenesis 9 signalosome COP9 Signalosome Complex - genetics COP9 Signalosome Complex - metabolism food chemistry Fungal Proteins - genetics Fungal Proteins - metabolism fungi Gene Expression Regulation, Fungal genes Light Magnaporthe oryzae metabolites Oryza - genetics Oryza - metabolism Oryza - microbiology pathogenesis photomorphogenesis physiological transport Plant Diseases - microbiology ubiquitination vegetative growth |
| title | Translocon Subunits of the COP9 Signalosome Complex Are a Central Hub for Regulating Multiple Photoresponsive Processes and Autophagic Flux in Magnaporthe oryzae |
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