Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins.
In C. elegans, 283 clec genes encode a highly diverse family of C-type lectin-like domain (CTLD) proteins. Since vertebrate CTLD proteins have characterized functions in defense responses against pathogens and since expression of C. elegans clec genes is pathogen-dependent, it is generally assumed t...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2021-04-01
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| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1009454 |
| _version_ | 1819176467557253120 |
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| author | Barbara Pees Wentao Yang Anke Kloock Carola Petersen Lena Peters Li Fan Meike Friedrichsen Sabrina Butze Alejandra Zárate-Potes Hinrich Schulenburg Katja Dierking |
| author_facet | Barbara Pees Wentao Yang Anke Kloock Carola Petersen Lena Peters Li Fan Meike Friedrichsen Sabrina Butze Alejandra Zárate-Potes Hinrich Schulenburg Katja Dierking |
| author_sort | Barbara Pees |
| collection | DOAJ |
| description | In C. elegans, 283 clec genes encode a highly diverse family of C-type lectin-like domain (CTLD) proteins. Since vertebrate CTLD proteins have characterized functions in defense responses against pathogens and since expression of C. elegans clec genes is pathogen-dependent, it is generally assumed that clec genes function in C. elegans immune defenses. However, little is known about the relative contribution and exact function of CLEC proteins in C. elegans immunity. Here, we focused on the C. elegans clec gene clec-4, whose expression is highly upregulated by pathogen infection, and its paralogs clec-41 and clec-42. We found that, while mutation of clec-4 resulted in enhanced resistance to the Gram-positive pathogen Bacillus thuringiensis MYBt18247 (Bt247), inactivation of clec-41 and clec-42 by RNAi enhanced susceptibility to Bt247. Further analyses revealed that enhanced resistance of clec-4 mutants to Bt247 was due to an increase in feeding cessation on the pathogen and consequently a decrease in pathogen load. Moreover, clec-4 mutants exhibited feeding deficits also on non-pathogenic bacteria that were in part reflected in the clec-4 gene expression profile, which overlapped with gene sets affected by starvation or mutation in nutrient sensing pathways. However, loss of CLEC-4 function only mildly affected life-history traits such as fertility, indicating that clec-4 mutants are not subjected to dietary restriction. While CLEC-4 function appears to be associated with the regulation of feeding behavior, we show that CLEC-41 and CLEC-42 proteins likely function as bona fide immune effector proteins that have bacterial binding and antimicrobial capacities. Together, our results exemplify functional diversification within clec gene paralogs. |
| first_indexed | 2024-12-22T21:11:14Z |
| format | Article |
| id | doaj.art-34c977ca4f7b4805806514e37704d14c |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-22T21:11:14Z |
| publishDate | 2021-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-34c977ca4f7b4805806514e37704d14c2022-12-21T18:12:31ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742021-04-01174e100945410.1371/journal.ppat.1009454Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins.Barbara PeesWentao YangAnke KloockCarola PetersenLena PetersLi FanMeike FriedrichsenSabrina ButzeAlejandra Zárate-PotesHinrich SchulenburgKatja DierkingIn C. elegans, 283 clec genes encode a highly diverse family of C-type lectin-like domain (CTLD) proteins. Since vertebrate CTLD proteins have characterized functions in defense responses against pathogens and since expression of C. elegans clec genes is pathogen-dependent, it is generally assumed that clec genes function in C. elegans immune defenses. However, little is known about the relative contribution and exact function of CLEC proteins in C. elegans immunity. Here, we focused on the C. elegans clec gene clec-4, whose expression is highly upregulated by pathogen infection, and its paralogs clec-41 and clec-42. We found that, while mutation of clec-4 resulted in enhanced resistance to the Gram-positive pathogen Bacillus thuringiensis MYBt18247 (Bt247), inactivation of clec-41 and clec-42 by RNAi enhanced susceptibility to Bt247. Further analyses revealed that enhanced resistance of clec-4 mutants to Bt247 was due to an increase in feeding cessation on the pathogen and consequently a decrease in pathogen load. Moreover, clec-4 mutants exhibited feeding deficits also on non-pathogenic bacteria that were in part reflected in the clec-4 gene expression profile, which overlapped with gene sets affected by starvation or mutation in nutrient sensing pathways. However, loss of CLEC-4 function only mildly affected life-history traits such as fertility, indicating that clec-4 mutants are not subjected to dietary restriction. While CLEC-4 function appears to be associated with the regulation of feeding behavior, we show that CLEC-41 and CLEC-42 proteins likely function as bona fide immune effector proteins that have bacterial binding and antimicrobial capacities. Together, our results exemplify functional diversification within clec gene paralogs.https://doi.org/10.1371/journal.ppat.1009454 |
| spellingShingle | Barbara Pees Wentao Yang Anke Kloock Carola Petersen Lena Peters Li Fan Meike Friedrichsen Sabrina Butze Alejandra Zárate-Potes Hinrich Schulenburg Katja Dierking Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins. PLoS Pathogens |
| title | Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins. |
| title_full | Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins. |
| title_fullStr | Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins. |
| title_full_unstemmed | Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins. |
| title_short | Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins. |
| title_sort | effector and regulator diverse functions of c elegans c type lectin like domain proteins |
| url | https://doi.org/10.1371/journal.ppat.1009454 |
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