Sex-linked deubiquitinase establishes uniparental transmission of chloroplast DNA

Sunjoo Joo, Thamali Kariyawasam, Minjae Kim, EonSeon Jin, Ursula Goodenough and Jae-Hyeok Lee ()
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Sunjoo Joo: University of British Columbia
Thamali Kariyawasam: University of British Columbia
Minjae Kim: Hanyang University
EonSeon Jin: Hanyang University
Ursula Goodenough: Washington University in St. Louis
Jae-Hyeok Lee: University of British Columbia

Nature Communications, 2022, vol. 13, issue 1, 1-12

Abstract: Abstract 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.

Date: 2022
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DOI: 10.1038/s41467-022-28807-6

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