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Magnaporthe oryzae endoplasmic reticulum membrane complex regulates the biogenesis of membrane proteins for pathogenicity
Summary In eukaryotes, the majority of newly synthesized integral membrane proteins are inserted into the endoplasmic reticulum (ER) membrane before transferred to their functional sites. The conserved ER membrane complex (EMC) takes part in the insertion process for tail‐anchored membrane proteins....
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| Published in: | The New phytologist 2023-05, Vol.238 (3), p.1163-1181 |
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| Main Authors: | , , , , , , , , , , , |
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| container_end_page | 1181 |
| container_issue | 3 |
| container_start_page | 1163 |
| container_title | The New phytologist |
| container_volume | 238 |
| creator | Liu, Ning Huang, Manna Liang, Xinyuan Cao, Miao Lun, Zhiqin Zhang, Yan Yang, Jun Bhadauria, Vijai Zhao, Wensheng Yan, Jiye Peng, You‐Liang Lu, Xunli |
| description | Summary
In eukaryotes, the majority of newly synthesized integral membrane proteins are inserted into the endoplasmic reticulum (ER) membrane before transferred to their functional sites. The conserved ER membrane complex (EMC) takes part in the insertion process for tail‐anchored membrane proteins. However, the function of EMC in phytopathogenic fungi has not been characterized.
Here, we report the identification and functional characterization of two EMC subunits MoEmc5 and MoEmc2 in Magnaporthe oryzae. The knockout mutants ΔMoemc5 and ΔMoemc2 exhibit substantial defect in autophagy, pathogenicity, cell wall integrity, and magnesium ion sensitivity.
We demonstrate that the autophagy process was severely impaired in the ΔMoemc5 and ΔMoemc2 mutants because of the low‐protein steady‐state level of Atg9, the sole membrane‐associated autophagy protein. Furthermore, the protein level of membrane proteins Chs4, Fks1, and MoMnr2 is also significantly reduced in the ΔMoemc5 and ΔMoemc2 strains, leading to their supersensitivity to Calcofluor white, Congo red, and magnesium. In addition, MoEmc5, but not MoEmc2, acts as a magnesium transporter independent of its EMC function.
Magnaporthe oryzae EMC regulates the biogenesis of membrane proteins for autophagy and virulence; therefore, EMC subunits could be potential targets for fungicide design in the future. |
| doi_str_mv | 10.1111/nph.18810 |
| format | article |
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In eukaryotes, the majority of newly synthesized integral membrane proteins are inserted into the endoplasmic reticulum (ER) membrane before transferred to their functional sites. The conserved ER membrane complex (EMC) takes part in the insertion process for tail‐anchored membrane proteins. However, the function of EMC in phytopathogenic fungi has not been characterized.
Here, we report the identification and functional characterization of two EMC subunits MoEmc5 and MoEmc2 in Magnaporthe oryzae. The knockout mutants ΔMoemc5 and ΔMoemc2 exhibit substantial defect in autophagy, pathogenicity, cell wall integrity, and magnesium ion sensitivity.
We demonstrate that the autophagy process was severely impaired in the ΔMoemc5 and ΔMoemc2 mutants because of the low‐protein steady‐state level of Atg9, the sole membrane‐associated autophagy protein. Furthermore, the protein level of membrane proteins Chs4, Fks1, and MoMnr2 is also significantly reduced in the ΔMoemc5 and ΔMoemc2 strains, leading to their supersensitivity to Calcofluor white, Congo red, and magnesium. In addition, MoEmc5, but not MoEmc2, acts as a magnesium transporter independent of its EMC function.
Magnaporthe oryzae EMC regulates the biogenesis of membrane proteins for autophagy and virulence; therefore, EMC subunits could be potential targets for fungicide design in the future.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.18810</identifier><identifier>PMID: 36772852</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Atg9 ; Autophagy ; Biogenesis ; Biosynthesis ; cell wall integrity ; Cell walls ; Chs4 ; Endoplasmic reticulum ; Endoplasmic Reticulum - metabolism ; Eukaryotes ; Fks1 ; Fungal Proteins - metabolism ; Fungi ; Fungicides ; Integral membrane proteins ; Magnaporthe ; Magnaporthe oryzae ; Magnesium ; Magnesium - metabolism ; magnesium transport ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Membranes ; Mnr2 ; MoEmc5 ; Mutants ; Oryza - metabolism ; Pathogenicity ; Pathogens ; Phytopathogenic fungi ; Plant Diseases - microbiology ; Proteins ; Virulence</subject><ispartof>The New phytologist, 2023-05, Vol.238 (3), p.1163-1181</ispartof><rights>2023 The Authors © 2023 New Phytologist Foundation</rights><rights>2023 The Authors New Phytologist © 2023 New Phytologist Foundation.</rights><rights>Copyright © 2023 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3130-4245bab41e48929997606f623a1c71d46587441ba06bb54b4077b6818fce593c3</cites><orcidid>0000-0002-3557-5475 ; 0000-0001-6360-3034 ; 0000-0002-1295-2143 ; 0000-0002-8610-1034 ; 0000-0003-4852-8106 ; 0000-0001-6085-9245</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36772852$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Ning</creatorcontrib><creatorcontrib>Huang, Manna</creatorcontrib><creatorcontrib>Liang, Xinyuan</creatorcontrib><creatorcontrib>Cao, Miao</creatorcontrib><creatorcontrib>Lun, Zhiqin</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Yang, Jun</creatorcontrib><creatorcontrib>Bhadauria, Vijai</creatorcontrib><creatorcontrib>Zhao, Wensheng</creatorcontrib><creatorcontrib>Yan, Jiye</creatorcontrib><creatorcontrib>Peng, You‐Liang</creatorcontrib><creatorcontrib>Lu, Xunli</creatorcontrib><title>Magnaporthe oryzae endoplasmic reticulum membrane complex regulates the biogenesis of membrane proteins for pathogenicity</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
In eukaryotes, the majority of newly synthesized integral membrane proteins are inserted into the endoplasmic reticulum (ER) membrane before transferred to their functional sites. The conserved ER membrane complex (EMC) takes part in the insertion process for tail‐anchored membrane proteins. However, the function of EMC in phytopathogenic fungi has not been characterized.
Here, we report the identification and functional characterization of two EMC subunits MoEmc5 and MoEmc2 in Magnaporthe oryzae. The knockout mutants ΔMoemc5 and ΔMoemc2 exhibit substantial defect in autophagy, pathogenicity, cell wall integrity, and magnesium ion sensitivity.
We demonstrate that the autophagy process was severely impaired in the ΔMoemc5 and ΔMoemc2 mutants because of the low‐protein steady‐state level of Atg9, the sole membrane‐associated autophagy protein. Furthermore, the protein level of membrane proteins Chs4, Fks1, and MoMnr2 is also significantly reduced in the ΔMoemc5 and ΔMoemc2 strains, leading to their supersensitivity to Calcofluor white, Congo red, and magnesium. In addition, MoEmc5, but not MoEmc2, acts as a magnesium transporter independent of its EMC function.
Magnaporthe oryzae EMC regulates the biogenesis of membrane proteins for autophagy and virulence; therefore, EMC subunits could be potential targets for fungicide design in the future.</description><subject>Atg9</subject><subject>Autophagy</subject><subject>Biogenesis</subject><subject>Biosynthesis</subject><subject>cell wall integrity</subject><subject>Cell walls</subject><subject>Chs4</subject><subject>Endoplasmic reticulum</subject><subject>Endoplasmic Reticulum - metabolism</subject><subject>Eukaryotes</subject><subject>Fks1</subject><subject>Fungal Proteins - metabolism</subject><subject>Fungi</subject><subject>Fungicides</subject><subject>Integral membrane proteins</subject><subject>Magnaporthe</subject><subject>Magnaporthe oryzae</subject><subject>Magnesium</subject><subject>Magnesium - metabolism</subject><subject>magnesium transport</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Membranes</subject><subject>Mnr2</subject><subject>MoEmc5</subject><subject>Mutants</subject><subject>Oryza - metabolism</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Phytopathogenic fungi</subject><subject>Plant Diseases - microbiology</subject><subject>Proteins</subject><subject>Virulence</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp10ctq3DAUBmBREppJ2kVfoAiyaRZOJFnWZVlCbpC0XbTQnZE0xzMKtuVKNqnz9NFkcoFAtNFCn34O50foCyXHNJ-TflgfU6Uo-YAWlAtdKFrKHbQghKlCcPF3D-2ndEsI0ZVgH9FeKaRkqmILNN-YVW-GEMc14BDnewMY-mUYWpM673CE0bupnTrcQWej6QG70A0t_M9Pq6k1IyS8-Wt9WEEPySccmlc8xDCC7xNuQsSDGdcb5Z0f509otzFtgs9P9wH6c372-_SyuP55cXX6_bpwJS1JwRmvrLGcAleaaa2lIKIRrDTUSbrkolKSc2oNEdZW3HIipRWKqsZBpUtXHqBv29w8yr8J0lh3Pjlo2zxemFLNpMxLYZqUmR6-obdhin2eLivNmBBEbdTRVrkYUorQ1EP0nYlzTUm96aPOfdSPfWT79Slxsh0sX-RzARmcbMGdb2F-P6n-8etyG_kAGsCV0g</recordid><startdate>202305</startdate><enddate>202305</enddate><creator>Liu, Ning</creator><creator>Huang, Manna</creator><creator>Liang, Xinyuan</creator><creator>Cao, Miao</creator><creator>Lun, Zhiqin</creator><creator>Zhang, Yan</creator><creator>Yang, Jun</creator><creator>Bhadauria, Vijai</creator><creator>Zhao, Wensheng</creator><creator>Yan, Jiye</creator><creator>Peng, You‐Liang</creator><creator>Lu, Xunli</creator><general>Wiley Subscription Services, Inc</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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3557-5475</orcidid><orcidid>https://orcid.org/0000-0001-6360-3034</orcidid><orcidid>https://orcid.org/0000-0002-1295-2143</orcidid><orcidid>https://orcid.org/0000-0002-8610-1034</orcidid><orcidid>https://orcid.org/0000-0003-4852-8106</orcidid><orcidid>https://orcid.org/0000-0001-6085-9245</orcidid></search><sort><creationdate>202305</creationdate><title>Magnaporthe oryzae endoplasmic reticulum membrane complex regulates the biogenesis of membrane proteins for pathogenicity</title><author>Liu, Ning ; Huang, Manna ; Liang, Xinyuan ; Cao, Miao ; Lun, Zhiqin ; Zhang, Yan ; Yang, Jun ; Bhadauria, Vijai ; Zhao, Wensheng ; Yan, Jiye ; Peng, You‐Liang ; Lu, Xunli</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3130-4245bab41e48929997606f623a1c71d46587441ba06bb54b4077b6818fce593c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Atg9</topic><topic>Autophagy</topic><topic>Biogenesis</topic><topic>Biosynthesis</topic><topic>cell wall integrity</topic><topic>Cell walls</topic><topic>Chs4</topic><topic>Endoplasmic reticulum</topic><topic>Endoplasmic Reticulum - metabolism</topic><topic>Eukaryotes</topic><topic>Fks1</topic><topic>Fungal Proteins - metabolism</topic><topic>Fungi</topic><topic>Fungicides</topic><topic>Integral membrane proteins</topic><topic>Magnaporthe</topic><topic>Magnaporthe oryzae</topic><topic>Magnesium</topic><topic>Magnesium - metabolism</topic><topic>magnesium transport</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Membranes</topic><topic>Mnr2</topic><topic>MoEmc5</topic><topic>Mutants</topic><topic>Oryza - metabolism</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Phytopathogenic fungi</topic><topic>Plant Diseases - microbiology</topic><topic>Proteins</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Ning</creatorcontrib><creatorcontrib>Huang, Manna</creatorcontrib><creatorcontrib>Liang, Xinyuan</creatorcontrib><creatorcontrib>Cao, Miao</creatorcontrib><creatorcontrib>Lun, Zhiqin</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Yang, Jun</creatorcontrib><creatorcontrib>Bhadauria, Vijai</creatorcontrib><creatorcontrib>Zhao, Wensheng</creatorcontrib><creatorcontrib>Yan, Jiye</creatorcontrib><creatorcontrib>Peng, You‐Liang</creatorcontrib><creatorcontrib>Lu, Xunli</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Ning</au><au>Huang, Manna</au><au>Liang, Xinyuan</au><au>Cao, Miao</au><au>Lun, Zhiqin</au><au>Zhang, Yan</au><au>Yang, Jun</au><au>Bhadauria, Vijai</au><au>Zhao, Wensheng</au><au>Yan, Jiye</au><au>Peng, You‐Liang</au><au>Lu, Xunli</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Magnaporthe oryzae endoplasmic reticulum membrane complex regulates the biogenesis of membrane proteins for pathogenicity</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2023-05</date><risdate>2023</risdate><volume>238</volume><issue>3</issue><spage>1163</spage><epage>1181</epage><pages>1163-1181</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
In eukaryotes, the majority of newly synthesized integral membrane proteins are inserted into the endoplasmic reticulum (ER) membrane before transferred to their functional sites. The conserved ER membrane complex (EMC) takes part in the insertion process for tail‐anchored membrane proteins. However, the function of EMC in phytopathogenic fungi has not been characterized.
Here, we report the identification and functional characterization of two EMC subunits MoEmc5 and MoEmc2 in Magnaporthe oryzae. The knockout mutants ΔMoemc5 and ΔMoemc2 exhibit substantial defect in autophagy, pathogenicity, cell wall integrity, and magnesium ion sensitivity.
We demonstrate that the autophagy process was severely impaired in the ΔMoemc5 and ΔMoemc2 mutants because of the low‐protein steady‐state level of Atg9, the sole membrane‐associated autophagy protein. Furthermore, the protein level of membrane proteins Chs4, Fks1, and MoMnr2 is also significantly reduced in the ΔMoemc5 and ΔMoemc2 strains, leading to their supersensitivity to Calcofluor white, Congo red, and magnesium. In addition, MoEmc5, but not MoEmc2, acts as a magnesium transporter independent of its EMC function.
Magnaporthe oryzae EMC regulates the biogenesis of membrane proteins for autophagy and virulence; therefore, EMC subunits could be potential targets for fungicide design in the future.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>36772852</pmid><doi>10.1111/nph.18810</doi><tpages>1181</tpages><orcidid>https://orcid.org/0000-0002-3557-5475</orcidid><orcidid>https://orcid.org/0000-0001-6360-3034</orcidid><orcidid>https://orcid.org/0000-0002-1295-2143</orcidid><orcidid>https://orcid.org/0000-0002-8610-1034</orcidid><orcidid>https://orcid.org/0000-0003-4852-8106</orcidid><orcidid>https://orcid.org/0000-0001-6085-9245</orcidid></addata></record> |
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| subjects | Atg9 Autophagy Biogenesis Biosynthesis cell wall integrity Cell walls Chs4 Endoplasmic reticulum Endoplasmic Reticulum - metabolism Eukaryotes Fks1 Fungal Proteins - metabolism Fungi Fungicides Integral membrane proteins Magnaporthe Magnaporthe oryzae Magnesium Magnesium - metabolism magnesium transport Membrane Proteins - genetics Membrane Proteins - metabolism Membranes Mnr2 MoEmc5 Mutants Oryza - metabolism Pathogenicity Pathogens Phytopathogenic fungi Plant Diseases - microbiology Proteins Virulence |
| title | Magnaporthe oryzae endoplasmic reticulum membrane complex regulates the biogenesis of membrane proteins for pathogenicity |
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