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Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA
Most sexual organisms inherit organelles from one parent, commonly by excluding organelles from the smaller gametes. However, post-mating elimination of organelles derived from one gamete ensures uniparental inheritance, where the underlying mechanisms to distinguish organelles by their origin remai...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8894339/ https://www.ncbi.nlm.nih.gov/pubmed/35241655 http://dx.doi.org/10.1038/s41467-022-28807-6 |
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author | Joo, Sunjoo Kariyawasam, Thamali Kim, Minjae Jin, EonSeon Goodenough, Ursula Lee, Jae-Hyeok |
author_facet | Joo, Sunjoo Kariyawasam, Thamali Kim, Minjae Jin, EonSeon Goodenough, Ursula Lee, Jae-Hyeok |
author_sort | Joo, Sunjoo |
collection | PubMed |
description | Most sexual organisms inherit organelles from one parent, commonly by excluding organelles from the smaller gametes. However, post-mating elimination of organelles derived from one gamete ensures uniparental inheritance, where the underlying mechanisms to distinguish organelles by their origin remain obscure. Mating in Chlamydomonas reinhardtii combines isomorphic plus and minus gametes, but chloroplast DNA from minus gametes is selectively degraded in zygotes. Here, we identify OTU2p (otubain protein 2), encoded in the plus mating-type locus MT+, as the protector of plus chloroplast. Otu2p is an otubain-like deubiquitinase, which prevents proteasome-mediated degradation of the preprotein translocase of the outer chloroplast membrane (TOC) during gametogenesis. Using OTU2p-knockouts and proteasome inhibitor treatment, we successfully redirect selective DNA degradation in chloroplasts with reduced TOC levels regardless of mating type, demonstrating that plus-specific Otu2p establishes uniparental chloroplast DNA inheritance. Our work documents that a sex-linked organelle quality control mechanism drives the uniparental organelle inheritance without dimorphic gametes. |
format | Online Article Text |
id | pubmed-8894339 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-88943392022-03-17 Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA Joo, Sunjoo Kariyawasam, Thamali Kim, Minjae Jin, EonSeon Goodenough, Ursula Lee, Jae-Hyeok Nat Commun Article Most sexual organisms inherit organelles from one parent, commonly by excluding organelles from the smaller gametes. However, post-mating elimination of organelles derived from one gamete ensures uniparental inheritance, where the underlying mechanisms to distinguish organelles by their origin remain obscure. Mating in Chlamydomonas reinhardtii combines isomorphic plus and minus gametes, but chloroplast DNA from minus gametes is selectively degraded in zygotes. Here, we identify OTU2p (otubain protein 2), encoded in the plus mating-type locus MT+, as the protector of plus chloroplast. Otu2p is an otubain-like deubiquitinase, which prevents proteasome-mediated degradation of the preprotein translocase of the outer chloroplast membrane (TOC) during gametogenesis. Using OTU2p-knockouts and proteasome inhibitor treatment, we successfully redirect selective DNA degradation in chloroplasts with reduced TOC levels regardless of mating type, demonstrating that plus-specific Otu2p establishes uniparental chloroplast DNA inheritance. Our work documents that a sex-linked organelle quality control mechanism drives the uniparental organelle inheritance without dimorphic gametes. Nature Publishing Group UK 2022-03-03 /pmc/articles/PMC8894339/ /pubmed/35241655 http://dx.doi.org/10.1038/s41467-022-28807-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Joo, Sunjoo Kariyawasam, Thamali Kim, Minjae Jin, EonSeon Goodenough, Ursula Lee, Jae-Hyeok Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA |
title | Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA |
title_full | Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA |
title_fullStr | Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA |
title_full_unstemmed | Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA |
title_short | Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA |
title_sort | sex-linked deubiquitinase establishes uniparental transmission of chloroplast dna |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8894339/ https://www.ncbi.nlm.nih.gov/pubmed/35241655 http://dx.doi.org/10.1038/s41467-022-28807-6 |
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