An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development
Most actin-related proteins (Arps) are highly conserved and carry out well-defined cellular functions in eukaryotes. However, many lineages like Drosophila and mammals encode divergent non-canonical Arps whose roles remain unknown. To elucidate the function of non-canonical Arps, we focus on Arp53D,...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-07-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/71279 |
| _version_ | 1797997480829255680 |
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| author | Courtney M Schroeder Sarah A Tomlin Isabel Mejia Natividad John R Valenzuela Janet M Young Harmit S Malik |
| author_facet | Courtney M Schroeder Sarah A Tomlin Isabel Mejia Natividad John R Valenzuela Janet M Young Harmit S Malik |
| author_sort | Courtney M Schroeder |
| collection | DOAJ |
| description | Most actin-related proteins (Arps) are highly conserved and carry out well-defined cellular functions in eukaryotes. However, many lineages like Drosophila and mammals encode divergent non-canonical Arps whose roles remain unknown. To elucidate the function of non-canonical Arps, we focus on Arp53D, which is highly expressed in testes and retained throughout Drosophila evolution. We show that Arp53D localizes to fusomes and actin cones, two germline-specific actin structures critical for sperm maturation, via a unique N-terminal tail. Surprisingly, we find that male fertility is not impaired upon Arp53D loss, yet population cage experiments reveal that Arp53D is required for optimal fitness in Drosophila melanogaster. To reconcile these findings, we focus on Arp53D function in ovaries and embryos where it is only weakly expressed. We find that under heat stress Arp53D-knockout (KO) females lay embryos with reduced nuclear integrity and lower viability; these defects are further exacerbated in Arp53D-KO embryos. Thus, despite its relatively recent evolution and primarily testis-specific expression, non-canonical Arp53D is required for optimal embryonic development in Drosophila. |
| first_indexed | 2024-04-11T10:33:40Z |
| format | Article |
| id | doaj.art-66f339a7be314fdaa5bcaa648a184beb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:33:40Z |
| publishDate | 2021-07-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj.art-66f339a7be314fdaa5bcaa648a184beb2022-12-22T04:29:21ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.71279An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic developmentCourtney M Schroeder0https://orcid.org/0000-0002-4526-8321Sarah A Tomlin1Isabel Mejia Natividad2John R Valenzuela3Janet M Young4https://orcid.org/0000-0001-8220-8427Harmit S Malik5https://orcid.org/0000-0001-6005-0016Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States; Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States; Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United StatesDivision of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States; Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, United StatesMost actin-related proteins (Arps) are highly conserved and carry out well-defined cellular functions in eukaryotes. However, many lineages like Drosophila and mammals encode divergent non-canonical Arps whose roles remain unknown. To elucidate the function of non-canonical Arps, we focus on Arp53D, which is highly expressed in testes and retained throughout Drosophila evolution. We show that Arp53D localizes to fusomes and actin cones, two germline-specific actin structures critical for sperm maturation, via a unique N-terminal tail. Surprisingly, we find that male fertility is not impaired upon Arp53D loss, yet population cage experiments reveal that Arp53D is required for optimal fitness in Drosophila melanogaster. To reconcile these findings, we focus on Arp53D function in ovaries and embryos where it is only weakly expressed. We find that under heat stress Arp53D-knockout (KO) females lay embryos with reduced nuclear integrity and lower viability; these defects are further exacerbated in Arp53D-KO embryos. Thus, despite its relatively recent evolution and primarily testis-specific expression, non-canonical Arp53D is required for optimal embryonic development in Drosophila.https://elifesciences.org/articles/71279actincytoskeletonDrosophilafertilitydevelopmentevolution |
| spellingShingle | Courtney M Schroeder Sarah A Tomlin Isabel Mejia Natividad John R Valenzuela Janet M Young Harmit S Malik An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development eLife actin cytoskeleton Drosophila fertility development evolution |
| title | An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development |
| title_full | An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development |
| title_fullStr | An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development |
| title_full_unstemmed | An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development |
| title_short | An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development |
| title_sort | actin related protein that is most highly expressed in drosophila testes is critical for embryonic development |
| topic | actin cytoskeleton Drosophila fertility development evolution |
| url | https://elifesciences.org/articles/71279 |
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