Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i>
Cyclophilin (Cyp) and Ca<sup>2+</sup>/calcineurin proteins are cellular components related to fungal morphogenesis and virulence; however, their roles in mediating the pathogenesis of <i>Botrytis cinerea</i>, the causative agent of gray mold on over 1000 plant species, remain...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-02-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/22/4/1694 |
| _version_ | 1797412865211105280 |
|---|---|
| author | Jiao Sun Chen-Hao Sun Hao-Wu Chang Song Yang Yue Liu Ming-Zhe Zhang Jie Hou Hao Zhang Gui-Hua Li Qing-Ming Qin |
| author_facet | Jiao Sun Chen-Hao Sun Hao-Wu Chang Song Yang Yue Liu Ming-Zhe Zhang Jie Hou Hao Zhang Gui-Hua Li Qing-Ming Qin |
| author_sort | Jiao Sun |
| collection | DOAJ |
| description | Cyclophilin (Cyp) and Ca<sup>2+</sup>/calcineurin proteins are cellular components related to fungal morphogenesis and virulence; however, their roles in mediating the pathogenesis of <i>Botrytis cinerea</i>, the causative agent of gray mold on over 1000 plant species, remain largely unexplored. Here, we show that disruption of cyclophilin gene <i>BcCYP2</i> did not impair the pathogen mycelial growth, osmotic and oxidative stress adaptation as well as cell wall integrity, but delayed conidial germination and germling development, altered conidial and sclerotial morphology, reduced infection cushion (IC) formation, sclerotial production and virulence. Exogenous cyclic adenosine monophosphate (cAMP) rescued the deficiency of IC formation of the ∆<i>Bccyp2</i> mutants, and exogenous cyclosporine A (CsA), an inhibitor targeting cyclophilins, altered hyphal morphology and prevented host-cell penetration in the <i>BcCYP2</i> harboring strains. Moreover, calcineurin-dependent (CND) genes are differentially expressed in strains losing <i>BcCYP2</i> in the presence of CsA, suggesting that BcCyp2 functions in the upstream of cAMP- and Ca<sup>2+</sup>/calcineurin-dependent signaling pathways. Interestingly, during IC formation, expression of <i>BcCYP2</i> is downregulated in a mutant losing <i>BcJAR1</i>, a gene encoding histone 3 lysine 4 (H3K4) demethylase that regulates fungal development and pathogenesis, in <i>B. cinerea</i>, implying that BcCyp2 functions under the control of BcJar1. Collectively, our findings provide new insights into cyclophilins mediating the pathogenesis of <i>B. cinerea</i> and potential targets for drug intervention for fungal diseases. |
| first_indexed | 2024-03-09T05:09:26Z |
| format | Article |
| id | doaj.art-cf5f35e8c8564ef6927b31dc623d6f11 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T05:09:26Z |
| publishDate | 2021-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-cf5f35e8c8564ef6927b31dc623d6f112023-12-03T12:51:23ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-02-01224169410.3390/ijms22041694Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i>Jiao Sun0Chen-Hao Sun1Hao-Wu Chang2Song Yang3Yue Liu4Ming-Zhe Zhang5Jie Hou6Hao Zhang7Gui-Hua Li8Qing-Ming Qin9College of Plant Sciences, Key Laboratory of Zoonosis Research, Ministry of Education, Jilin University, Changchun 130062, ChinaCollege of Plant Sciences, Jilin University, Changchun 130062, ChinaKey Laboratory of Symbolic Computation and Knowledge Engineering, Ministry of Education, College of Computer Science and Technology, Jilin University, Changchun 130012, ChinaCollege of Plant Sciences, Jilin University, Changchun 130062, ChinaCollege of Plant Sciences, Key Laboratory of Zoonosis Research, Ministry of Education, Jilin University, Changchun 130062, ChinaCollege of Plant Sciences, Jilin University, Changchun 130062, ChinaCollege of Plant Sciences, Key Laboratory of Zoonosis Research, Ministry of Education, Jilin University, Changchun 130062, ChinaKey Laboratory of Symbolic Computation and Knowledge Engineering, Ministry of Education, College of Computer Science and Technology, Jilin University, Changchun 130012, ChinaCollege of Plant Sciences, Jilin University, Changchun 130062, ChinaCollege of Plant Sciences, Key Laboratory of Zoonosis Research, Ministry of Education, Jilin University, Changchun 130062, ChinaCyclophilin (Cyp) and Ca<sup>2+</sup>/calcineurin proteins are cellular components related to fungal morphogenesis and virulence; however, their roles in mediating the pathogenesis of <i>Botrytis cinerea</i>, the causative agent of gray mold on over 1000 plant species, remain largely unexplored. Here, we show that disruption of cyclophilin gene <i>BcCYP2</i> did not impair the pathogen mycelial growth, osmotic and oxidative stress adaptation as well as cell wall integrity, but delayed conidial germination and germling development, altered conidial and sclerotial morphology, reduced infection cushion (IC) formation, sclerotial production and virulence. Exogenous cyclic adenosine monophosphate (cAMP) rescued the deficiency of IC formation of the ∆<i>Bccyp2</i> mutants, and exogenous cyclosporine A (CsA), an inhibitor targeting cyclophilins, altered hyphal morphology and prevented host-cell penetration in the <i>BcCYP2</i> harboring strains. Moreover, calcineurin-dependent (CND) genes are differentially expressed in strains losing <i>BcCYP2</i> in the presence of CsA, suggesting that BcCyp2 functions in the upstream of cAMP- and Ca<sup>2+</sup>/calcineurin-dependent signaling pathways. Interestingly, during IC formation, expression of <i>BcCYP2</i> is downregulated in a mutant losing <i>BcJAR1</i>, a gene encoding histone 3 lysine 4 (H3K4) demethylase that regulates fungal development and pathogenesis, in <i>B. cinerea</i>, implying that BcCyp2 functions under the control of BcJar1. Collectively, our findings provide new insights into cyclophilins mediating the pathogenesis of <i>B. cinerea</i> and potential targets for drug intervention for fungal diseases.https://www.mdpi.com/1422-0067/22/4/1694<i>Botrytis cinerea</i>cyclophilincalcineurinmorphogenesisinfection structure formationpathogenesis |
| spellingShingle | Jiao Sun Chen-Hao Sun Hao-Wu Chang Song Yang Yue Liu Ming-Zhe Zhang Jie Hou Hao Zhang Gui-Hua Li Qing-Ming Qin Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i> International Journal of Molecular Sciences <i>Botrytis cinerea</i> cyclophilin calcineurin morphogenesis infection structure formation pathogenesis |
| title | Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i> |
| title_full | Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i> |
| title_fullStr | Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i> |
| title_full_unstemmed | Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i> |
| title_short | Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus <i>Botrytis cinerea</i> |
| title_sort | cyclophilin bccyp2 regulates infection related development to facilitate virulence of the gray mold fungus i botrytis cinerea i |
| topic | <i>Botrytis cinerea</i> cyclophilin calcineurin morphogenesis infection structure formation pathogenesis |
| url | https://www.mdpi.com/1422-0067/22/4/1694 |
| work_keys_str_mv | AT jiaosun cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT chenhaosun cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT haowuchang cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT songyang cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT yueliu cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT mingzhezhang cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT jiehou cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT haozhang cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT guihuali cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai AT qingmingqin cyclophilinbccyp2regulatesinfectionrelateddevelopmenttofacilitatevirulenceofthegraymoldfungusibotrytiscinereai |