Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Joo, Sunjoo, Kariyawasam, Thamali, Kim, Minjae, Jin, EonSeon, Goodenough, Ursula, Lee, Jae-Hyeok
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
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
_version_ 1784662636170838016
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
work_keys_str_mv AT joosunjoo sexlinkeddeubiquitinaseestablishesuniparentaltransmissionofchloroplastdna
AT kariyawasamthamali sexlinkeddeubiquitinaseestablishesuniparentaltransmissionofchloroplastdna
AT kimminjae sexlinkeddeubiquitinaseestablishesuniparentaltransmissionofchloroplastdna
AT jineonseon sexlinkeddeubiquitinaseestablishesuniparentaltransmissionofchloroplastdna
AT goodenoughursula sexlinkeddeubiquitinaseestablishesuniparentaltransmissionofchloroplastdna
AT leejaehyeok sexlinkeddeubiquitinaseestablishesuniparentaltransmissionofchloroplastdna