Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development
Fungal sexual development requires the involvement of a large number of functional genes. Fungal genes encoding sexual differentiation process proteins (SDPs), isps, have been known for decades. isp4/SDP and its homologs function as oligopeptide transporters (OPTs), yet their roles in reproduction a...
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Frontiers Media S.A.
2020-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.02994/full |
| _version_ | 1819139873065402368 |
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| author | Xiang-Li Xie Yi Wei Yan-Yue Song Guan-Ming Pan Li-Na Chen Gang Wang Shi-Hong Zhang |
| author_facet | Xiang-Li Xie Yi Wei Yan-Yue Song Guan-Ming Pan Li-Na Chen Gang Wang Shi-Hong Zhang |
| author_sort | Xiang-Li Xie |
| collection | DOAJ |
| description | Fungal sexual development requires the involvement of a large number of functional genes. Fungal genes encoding sexual differentiation process proteins (SDPs), isps, have been known for decades. isp4/SDP and its homologs function as oligopeptide transporters (OPTs), yet their roles in reproduction are unknown. Here, we genetically analyzed all four isp4/SDP homologs in the sexual species Chaetomium thermophilum and asexual species Thermomyces lanuginosus. Using single gene deletion mutants, we found that T. lanuginosus SDP (TlSDP) participated in asexual sporulation, whereas the other homologs participated in sexual morphogenesis. In complementary tests, C. thermophilum SDPs (CtSDP1-3) restored sporulation defects in TlSDP deletion strains (ΔTlSDP), and their translated proteins, which were localized onto the cytomembrane, possessed OPT activity. Interestingly, CtSDP2 accumulated at the top of the hyphae played a distinct role in determining the sexual cycle, glutathione transport, and lifespan shortening. A unique 72nt-insertion fragment (72INS) was discovered in CtSDP2. Biological analysis of the 72INS deletion and DsRED-tagged fusion strains implied the involvement of 72INS in fungal growth and development. In contrast to TlSDP, which only contributes to conidial production, the three CtSDPs play important roles in sexual and asexual reproduction, and CtSDP2 harbors a unique functional 72INS that initiates sexual morphogenesis. |
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| id | doaj.art-96cf65a4f70b4b328bb2a0be67a4903a |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-22T11:29:34Z |
| publishDate | 2020-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-96cf65a4f70b4b328bb2a0be67a4903a2022-12-21T18:27:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-01-011010.3389/fmicb.2019.02994506724Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in DevelopmentXiang-Li Xie0Yi Wei1Yan-Yue Song2Guan-Ming Pan3Li-Na Chen4Gang Wang5Shi-Hong Zhang6College of Plant Sciences, Jilin University, Changchun, ChinaCollege of Plant Sciences, Jilin University, Changchun, ChinaCollege of Plant Sciences, Jilin University, Changchun, ChinaCollege of Plant Sciences, Jilin University, Changchun, ChinaCollege of Plant Sciences, Jilin University, Changchun, ChinaSchool of Life Sciences, Henan University, Kaifeng, ChinaCollege of Plant Sciences, Jilin University, Changchun, ChinaFungal sexual development requires the involvement of a large number of functional genes. Fungal genes encoding sexual differentiation process proteins (SDPs), isps, have been known for decades. isp4/SDP and its homologs function as oligopeptide transporters (OPTs), yet their roles in reproduction are unknown. Here, we genetically analyzed all four isp4/SDP homologs in the sexual species Chaetomium thermophilum and asexual species Thermomyces lanuginosus. Using single gene deletion mutants, we found that T. lanuginosus SDP (TlSDP) participated in asexual sporulation, whereas the other homologs participated in sexual morphogenesis. In complementary tests, C. thermophilum SDPs (CtSDP1-3) restored sporulation defects in TlSDP deletion strains (ΔTlSDP), and their translated proteins, which were localized onto the cytomembrane, possessed OPT activity. Interestingly, CtSDP2 accumulated at the top of the hyphae played a distinct role in determining the sexual cycle, glutathione transport, and lifespan shortening. A unique 72nt-insertion fragment (72INS) was discovered in CtSDP2. Biological analysis of the 72INS deletion and DsRED-tagged fusion strains implied the involvement of 72INS in fungal growth and development. In contrast to TlSDP, which only contributes to conidial production, the three CtSDPs play important roles in sexual and asexual reproduction, and CtSDP2 harbors a unique functional 72INS that initiates sexual morphogenesis.https://www.frontiersin.org/article/10.3389/fmicb.2019.02994/fullisp4/SDP (sexual differentiation process protein)OPT (oligopeptide transporter)sexual reproduction72nt-insertion fragment (72INS)C. thermophilumT. lanuginosus |
| spellingShingle | Xiang-Li Xie Yi Wei Yan-Yue Song Guan-Ming Pan Li-Na Chen Gang Wang Shi-Hong Zhang Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development Frontiers in Microbiology isp4/SDP (sexual differentiation process protein) OPT (oligopeptide transporter) sexual reproduction 72nt-insertion fragment (72INS) C. thermophilum T. lanuginosus |
| title | Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development |
| title_full | Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development |
| title_fullStr | Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development |
| title_full_unstemmed | Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development |
| title_short | Genetic Analysis of Four Sexual Differentiation Process Proteins (isp4/SDPs) in Chaetomium thermophilum and Thermomyces lanuginosus Reveals Their Distinct Roles in Development |
| title_sort | genetic analysis of four sexual differentiation process proteins isp4 sdps in chaetomium thermophilum and thermomyces lanuginosus reveals their distinct roles in development |
| topic | isp4/SDP (sexual differentiation process protein) OPT (oligopeptide transporter) sexual reproduction 72nt-insertion fragment (72INS) C. thermophilum T. lanuginosus |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.02994/full |
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