MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae.
Actin organization is a conserved cellular process that regulates the growth and development of eukaryotic cells. It also governs the virulence process of pathogenic fungi, such as the rice blast fungus Magnaporthe oryzae, with mechanisms not yet fully understood. In a previous study, we found that...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2017-05-01
|
| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC5466339?pdf=render |
| _version_ | 1818128850042748928 |
|---|---|
| author | Lianwei Li Xiaolin Chen Shengpei Zhang Jun Yang Deng Chen Muxing Liu Haifeng Zhang Xiaobo Zheng Ping Wang Youliang Peng Zhengguang Zhang |
| author_facet | Lianwei Li Xiaolin Chen Shengpei Zhang Jun Yang Deng Chen Muxing Liu Haifeng Zhang Xiaobo Zheng Ping Wang Youliang Peng Zhengguang Zhang |
| author_sort | Lianwei Li |
| collection | DOAJ |
| description | Actin organization is a conserved cellular process that regulates the growth and development of eukaryotic cells. It also governs the virulence process of pathogenic fungi, such as the rice blast fungus Magnaporthe oryzae, with mechanisms not yet fully understood. In a previous study, we found that actin-regulating kinase MoArk1 displays conserved functions important in endocytosis and actin organization, and MoArk1 is required for maintaining the growth and full virulence of M. oryzae. To understand how MoArk1 might function, we identified capping protein homologs from M. oryzae (MoCAP) that interact with MoArk1 in vivo. MoCAP is heterodimer consisting of α and β subunits MoCapA and MoCapB. Single and double deletions of MoCAP subunits resulted in abnormal mycelial growth and conidia formation. The ΔMocap mutants also exhibited reduced appressorium penetration and invasive hyphal growth within host cells. Furthermore, the ΔMocap mutants exhibited delayed endocytosis and abnormal cytoskeleton assembly. Consistent with above findings, MoCAP proteins interacted with MoAct1, co-localized with actin during mycelial development, and participated in appressorial actin ring formation. Further analysis revealed that the S85 residue of MoCapA and the S285 residue of MoCapB were subject to phosphorylation by MoArk1 that negatively regulates MoCAP functions. Finally, the addition of exogenous phosphatidylinositol 4,5-bisphosphate (PIP2) failed to modulate actin ring formation in ΔMocap mutants, in contrast to the wild-type strain, suggesting that MoCAP may also mediate phospholipid signaling in the regulation of the actin organization. These results together demonstrate that MoCAP proteins whose functions are regulated by MoArk1 and PIP2 are important for endocytosis and actin dynamics that are directly linked to growth, conidiation and pathogenicity of M. oryzae. |
| first_indexed | 2024-12-11T07:39:48Z |
| format | Article |
| id | doaj.art-f5a6b2a54ab14fcfb9ec39fec23927af |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-11T07:39:48Z |
| publishDate | 2017-05-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-f5a6b2a54ab14fcfb9ec39fec23927af2022-12-22T01:15:36ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042017-05-01135e100681410.1371/journal.pgen.1006814MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae.Lianwei LiXiaolin ChenShengpei ZhangJun YangDeng ChenMuxing LiuHaifeng ZhangXiaobo ZhengPing WangYouliang PengZhengguang ZhangActin organization is a conserved cellular process that regulates the growth and development of eukaryotic cells. It also governs the virulence process of pathogenic fungi, such as the rice blast fungus Magnaporthe oryzae, with mechanisms not yet fully understood. In a previous study, we found that actin-regulating kinase MoArk1 displays conserved functions important in endocytosis and actin organization, and MoArk1 is required for maintaining the growth and full virulence of M. oryzae. To understand how MoArk1 might function, we identified capping protein homologs from M. oryzae (MoCAP) that interact with MoArk1 in vivo. MoCAP is heterodimer consisting of α and β subunits MoCapA and MoCapB. Single and double deletions of MoCAP subunits resulted in abnormal mycelial growth and conidia formation. The ΔMocap mutants also exhibited reduced appressorium penetration and invasive hyphal growth within host cells. Furthermore, the ΔMocap mutants exhibited delayed endocytosis and abnormal cytoskeleton assembly. Consistent with above findings, MoCAP proteins interacted with MoAct1, co-localized with actin during mycelial development, and participated in appressorial actin ring formation. Further analysis revealed that the S85 residue of MoCapA and the S285 residue of MoCapB were subject to phosphorylation by MoArk1 that negatively regulates MoCAP functions. Finally, the addition of exogenous phosphatidylinositol 4,5-bisphosphate (PIP2) failed to modulate actin ring formation in ΔMocap mutants, in contrast to the wild-type strain, suggesting that MoCAP may also mediate phospholipid signaling in the regulation of the actin organization. These results together demonstrate that MoCAP proteins whose functions are regulated by MoArk1 and PIP2 are important for endocytosis and actin dynamics that are directly linked to growth, conidiation and pathogenicity of M. oryzae.http://europepmc.org/articles/PMC5466339?pdf=render |
| spellingShingle | Lianwei Li Xiaolin Chen Shengpei Zhang Jun Yang Deng Chen Muxing Liu Haifeng Zhang Xiaobo Zheng Ping Wang Youliang Peng Zhengguang Zhang MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. PLoS Genetics |
| title | MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. |
| title_full | MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. |
| title_fullStr | MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. |
| title_full_unstemmed | MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. |
| title_short | MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. |
| title_sort | mocap proteins regulated by moark1 mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of magnaporthe oryzae |
| url | http://europepmc.org/articles/PMC5466339?pdf=render |
| work_keys_str_mv | AT lianweili mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT xiaolinchen mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT shengpeizhang mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT junyang mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT dengchen mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT muxingliu mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT haifengzhang mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT xiaobozheng mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT pingwang mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT youliangpeng mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae AT zhengguangzhang mocapproteinsregulatedbymoark1mediatedphosphorylationcoordinateendocytosisandactindynamicstogoverndevelopmentandvirulenceofmagnaportheoryzae |