Foisc1 regulates growth, conidiation, sensitivity to salicylic acid, and pathogenicity of Fusarium oxysporum f. sp. cubense tropical race 4
The secreted isochorismatases derived from certain filamentous pathogens play vital roles in the infection of host plants by lowering salicylic acid (SA) levels and suppressing SA-mediated defense pathway. However, it remains unclear whether the fungus Fusarium oxysporum f. sp. cubense tropical race...
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description | The secreted isochorismatases derived from certain filamentous pathogens play vital roles in the infection of host plants by lowering salicylic acid (SA) levels and suppressing SA-mediated defense pathway. However, it remains unclear whether the fungus Fusarium oxysporum f. sp. cubense tropical race 4 (FocTR4), which causes vascular wilt in bananas, utilizes isochorismatases to modulate SA levels in the host and subvert the banana defense system for successful infection. In the current study, we selected and functionally characterized the foisc1 gene, one of 10 putative isochorismatase-encoding genes in FocTR4 that showed significant upregulation during early stages of infection. Deletion of foisc1 resulted in enhanced vegetative growth and conidiation, increased sensitivity to SA, reduced colonization within host plants, as well as impaired pathogenicity. Conversely, complementation restored phenotypes similar to those observed in the wild-type strain. Furthermore, deletion of foisc1 led to a notable rise in activities of defense-related enzymes such as catalase, peroxidase, and phenylalnine ammonialyase; along with an upregulated expression of several defense-related genes including PR genes and NPR1 genes within hosts' tissues. The non-secretory nature of Foisc1 protein was confirmed and its absence did not affect SA levels within host plants. Transcriptome analysis revealed that deletion of foisc1 resulted in decreased expression levels for numerous genes associated with pathogenicity including those involved in fusaric acid biosynthesis and effector genes as well as a catechol 1,2-dioxygenase gene essential for SA degradation; while increasing expression levels for numerous genes associated with hyphal growth and conidiation were observed instead. Therefore, our findings suggest that Foisc1 may influence hyphal growth, conidiation, sensitivity to SA, and pathogenicity of FocTR4 through modulation of various genes implicated in these processes. These findings provide valuable insights into the pathogenesis of FocTR4, and create a groundwork for the future development of innovative control strategies targeting vascular wilt disease of banana.
•foisc1 encodes a non-secretory isochorismatase.•Foisc1 regulates growth, conidiation, and pathogenicity in FocTR4.•Foisc1 modulates the sensitivity to salicylic acid (SA) in FocTR4.•Numerous DEGs are related to growth, conidiation, sensitivity to SA and pathogenicity.•Foisc1 influences the expression of 11 genes i |
doi_str_mv | 10.1016/j.micres.2024.127975 |
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•foisc1 encodes a non-secretory isochorismatase.•Foisc1 regulates growth, conidiation, and pathogenicity in FocTR4.•Foisc1 modulates the sensitivity to salicylic acid (SA) in FocTR4.•Numerous DEGs are related to growth, conidiation, sensitivity to SA and pathogenicity.•Foisc1 influences the expression of 11 genes involved in fusaric acid biosynthesis.</description><identifier>ISSN: 0944-5013</identifier><identifier>ISSN: 1618-0623</identifier><identifier>EISSN: 1618-0623</identifier><identifier>DOI: 10.1016/j.micres.2024.127975</identifier><identifier>PMID: 39608178</identifier><language>eng</language><publisher>Germany: Elsevier GmbH</publisher><subject>Defense response ; Fungal Proteins - genetics ; Fungal Proteins - metabolism ; Fusaric acid biosynthesis ; Fusarium - genetics ; Fusarium - pathogenicity ; Gene Deletion ; Gene Expression Regulation, Fungal ; Isochorismatase ; Musa - microbiology ; Pathogenicity ; Plant Diseases - microbiology ; Salicylic acid ; Salicylic Acid - metabolism ; Spores, Fungal - genetics ; Spores, Fungal - growth & development ; Vascular wilt of banana ; Virulence</subject><ispartof>Microbiological research, 2025-02, Vol.291, p.127975, Article 127975</ispartof><rights>2024 Elsevier GmbH</rights><rights>Copyright © 2024 Elsevier GmbH. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c241t-7a3ba21eb30df2a71175b5fd8a91fd162acae6fe7579de80069597f78dba6c553</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.micres.2024.127975$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39608178$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guo, Lijia</creatorcontrib><creatorcontrib>Wang, Jun</creatorcontrib><creatorcontrib>Zhou, You</creatorcontrib><creatorcontrib>Liang, Changcong</creatorcontrib><creatorcontrib>Liu, Lei</creatorcontrib><creatorcontrib>Yang, Yang</creatorcontrib><creatorcontrib>Huang, Junsheng</creatorcontrib><creatorcontrib>Yang, Laying</creatorcontrib><title>Foisc1 regulates growth, conidiation, sensitivity to salicylic acid, and pathogenicity of Fusarium oxysporum f. sp. cubense tropical race 4</title><title>Microbiological research</title><addtitle>Microbiol Res</addtitle><description>The secreted isochorismatases derived from certain filamentous pathogens play vital roles in the infection of host plants by lowering salicylic acid (SA) levels and suppressing SA-mediated defense pathway. However, it remains unclear whether the fungus Fusarium oxysporum f. sp. cubense tropical race 4 (FocTR4), which causes vascular wilt in bananas, utilizes isochorismatases to modulate SA levels in the host and subvert the banana defense system for successful infection. In the current study, we selected and functionally characterized the foisc1 gene, one of 10 putative isochorismatase-encoding genes in FocTR4 that showed significant upregulation during early stages of infection. Deletion of foisc1 resulted in enhanced vegetative growth and conidiation, increased sensitivity to SA, reduced colonization within host plants, as well as impaired pathogenicity. Conversely, complementation restored phenotypes similar to those observed in the wild-type strain. Furthermore, deletion of foisc1 led to a notable rise in activities of defense-related enzymes such as catalase, peroxidase, and phenylalnine ammonialyase; along with an upregulated expression of several defense-related genes including PR genes and NPR1 genes within hosts' tissues. The non-secretory nature of Foisc1 protein was confirmed and its absence did not affect SA levels within host plants. Transcriptome analysis revealed that deletion of foisc1 resulted in decreased expression levels for numerous genes associated with pathogenicity including those involved in fusaric acid biosynthesis and effector genes as well as a catechol 1,2-dioxygenase gene essential for SA degradation; while increasing expression levels for numerous genes associated with hyphal growth and conidiation were observed instead. Therefore, our findings suggest that Foisc1 may influence hyphal growth, conidiation, sensitivity to SA, and pathogenicity of FocTR4 through modulation of various genes implicated in these processes. These findings provide valuable insights into the pathogenesis of FocTR4, and create a groundwork for the future development of innovative control strategies targeting vascular wilt disease of banana.
•foisc1 encodes a non-secretory isochorismatase.•Foisc1 regulates growth, conidiation, and pathogenicity in FocTR4.•Foisc1 modulates the sensitivity to salicylic acid (SA) in FocTR4.•Numerous DEGs are related to growth, conidiation, sensitivity to SA and pathogenicity.•Foisc1 influences the expression of 11 genes involved in fusaric acid biosynthesis.</description><subject>Defense response</subject><subject>Fungal Proteins - genetics</subject><subject>Fungal Proteins - metabolism</subject><subject>Fusaric acid biosynthesis</subject><subject>Fusarium - genetics</subject><subject>Fusarium - pathogenicity</subject><subject>Gene Deletion</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Isochorismatase</subject><subject>Musa - microbiology</subject><subject>Pathogenicity</subject><subject>Plant Diseases - microbiology</subject><subject>Salicylic acid</subject><subject>Salicylic Acid - metabolism</subject><subject>Spores, Fungal - genetics</subject><subject>Spores, Fungal - growth & development</subject><subject>Vascular wilt of banana</subject><subject>Virulence</subject><issn>0944-5013</issn><issn>1618-0623</issn><issn>1618-0623</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcFu1DAQhi0EotvCGyDkI4dNsJ3ETi5IqGIpUiUucLYm9njrVRIH2ynsM_DSZJXCkcNo5vDN_2vmJ-QNZyVnXL4_laM3EVMpmKhLLlSnmmdkxyVvCyZF9ZzsWFfXRcN4dUWuUzoxxuuuFS_JVdVJ1nLV7sjvQ_DJcBrxuAyQMdFjDD_zw56aMHnrIfsw7WnCKfnsH30-0xxogsGb81oUjLd7CpOlM-SHcMTJmwsUHD0sCaJfRhp-ndMc4jq5kqa5pGbpVz2kOYbZGxhoBIO0fkVeOBgSvn7qN-T74dO327vi_uvnL7cf7wsjap4LBVUPgmNfMesEKM5V0zfOttBxZ7kUYAClQ9WozmLLmOyaTjnV2h6kaZrqhrzbdOcYfiyYsh7XH-AwwIRhSbriVc1kI1u5ovWGmhhSiuj0HP0I8aw505cY9ElvMehLDHqLYV17--Sw9CPaf0t__74CHzYA1zsfPUadjMfJoPURTdY2-P87_AGAV51k</recordid><startdate>20250201</startdate><enddate>20250201</enddate><creator>Guo, Lijia</creator><creator>Wang, Jun</creator><creator>Zhou, You</creator><creator>Liang, Changcong</creator><creator>Liu, Lei</creator><creator>Yang, Yang</creator><creator>Huang, Junsheng</creator><creator>Yang, Laying</creator><general>Elsevier GmbH</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></search><sort><creationdate>20250201</creationdate><title>Foisc1 regulates growth, conidiation, sensitivity to salicylic acid, and pathogenicity of Fusarium oxysporum f. sp. cubense tropical race 4</title><author>Guo, Lijia ; Wang, Jun ; Zhou, You ; Liang, Changcong ; Liu, Lei ; Yang, Yang ; Huang, Junsheng ; Yang, Laying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c241t-7a3ba21eb30df2a71175b5fd8a91fd162acae6fe7579de80069597f78dba6c553</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>Defense response</topic><topic>Fungal Proteins - genetics</topic><topic>Fungal Proteins - metabolism</topic><topic>Fusaric acid biosynthesis</topic><topic>Fusarium - genetics</topic><topic>Fusarium - pathogenicity</topic><topic>Gene Deletion</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Isochorismatase</topic><topic>Musa - microbiology</topic><topic>Pathogenicity</topic><topic>Plant Diseases - microbiology</topic><topic>Salicylic acid</topic><topic>Salicylic Acid - metabolism</topic><topic>Spores, Fungal - genetics</topic><topic>Spores, Fungal - growth & development</topic><topic>Vascular wilt of banana</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guo, Lijia</creatorcontrib><creatorcontrib>Wang, Jun</creatorcontrib><creatorcontrib>Zhou, You</creatorcontrib><creatorcontrib>Liang, Changcong</creatorcontrib><creatorcontrib>Liu, Lei</creatorcontrib><creatorcontrib>Yang, Yang</creatorcontrib><creatorcontrib>Huang, Junsheng</creatorcontrib><creatorcontrib>Yang, Laying</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><jtitle>Microbiological research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guo, Lijia</au><au>Wang, Jun</au><au>Zhou, You</au><au>Liang, Changcong</au><au>Liu, Lei</au><au>Yang, Yang</au><au>Huang, Junsheng</au><au>Yang, Laying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Foisc1 regulates growth, conidiation, sensitivity to salicylic acid, and pathogenicity of Fusarium oxysporum f. sp. cubense tropical race 4</atitle><jtitle>Microbiological research</jtitle><addtitle>Microbiol Res</addtitle><date>2025-02-01</date><risdate>2025</risdate><volume>291</volume><spage>127975</spage><pages>127975-</pages><artnum>127975</artnum><issn>0944-5013</issn><issn>1618-0623</issn><eissn>1618-0623</eissn><abstract>The secreted isochorismatases derived from certain filamentous pathogens play vital roles in the infection of host plants by lowering salicylic acid (SA) levels and suppressing SA-mediated defense pathway. However, it remains unclear whether the fungus Fusarium oxysporum f. sp. cubense tropical race 4 (FocTR4), which causes vascular wilt in bananas, utilizes isochorismatases to modulate SA levels in the host and subvert the banana defense system for successful infection. In the current study, we selected and functionally characterized the foisc1 gene, one of 10 putative isochorismatase-encoding genes in FocTR4 that showed significant upregulation during early stages of infection. Deletion of foisc1 resulted in enhanced vegetative growth and conidiation, increased sensitivity to SA, reduced colonization within host plants, as well as impaired pathogenicity. Conversely, complementation restored phenotypes similar to those observed in the wild-type strain. Furthermore, deletion of foisc1 led to a notable rise in activities of defense-related enzymes such as catalase, peroxidase, and phenylalnine ammonialyase; along with an upregulated expression of several defense-related genes including PR genes and NPR1 genes within hosts' tissues. The non-secretory nature of Foisc1 protein was confirmed and its absence did not affect SA levels within host plants. Transcriptome analysis revealed that deletion of foisc1 resulted in decreased expression levels for numerous genes associated with pathogenicity including those involved in fusaric acid biosynthesis and effector genes as well as a catechol 1,2-dioxygenase gene essential for SA degradation; while increasing expression levels for numerous genes associated with hyphal growth and conidiation were observed instead. Therefore, our findings suggest that Foisc1 may influence hyphal growth, conidiation, sensitivity to SA, and pathogenicity of FocTR4 through modulation of various genes implicated in these processes. These findings provide valuable insights into the pathogenesis of FocTR4, and create a groundwork for the future development of innovative control strategies targeting vascular wilt disease of banana.
•foisc1 encodes a non-secretory isochorismatase.•Foisc1 regulates growth, conidiation, and pathogenicity in FocTR4.•Foisc1 modulates the sensitivity to salicylic acid (SA) in FocTR4.•Numerous DEGs are related to growth, conidiation, sensitivity to SA and pathogenicity.•Foisc1 influences the expression of 11 genes involved in fusaric acid biosynthesis.</abstract><cop>Germany</cop><pub>Elsevier GmbH</pub><pmid>39608178</pmid><doi>10.1016/j.micres.2024.127975</doi></addata></record> |
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subjects | Defense response Fungal Proteins - genetics Fungal Proteins - metabolism Fusaric acid biosynthesis Fusarium - genetics Fusarium - pathogenicity Gene Deletion Gene Expression Regulation, Fungal Isochorismatase Musa - microbiology Pathogenicity Plant Diseases - microbiology Salicylic acid Salicylic Acid - metabolism Spores, Fungal - genetics Spores, Fungal - growth & development Vascular wilt of banana Virulence |
title | Foisc1 regulates growth, conidiation, sensitivity to salicylic acid, and pathogenicity of Fusarium oxysporum f. sp. cubense tropical race 4 |
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