ZYP1-mediated recruitment of PCH2 to the synaptonemal complex remodels the chromosome axis leading to crossover restriction.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
09 12 2022
Historique:
accepted: 21 11 2022
revised: 15 11 2022
received: 02 04 2022
pubmed: 13 12 2022
medline: 11 1 2023
entrez: 12 12 2022
Statut: ppublish

Résumé

Chromosome axis-associated HORMA domain proteins (HORMADs), e.g. ASY1 in Arabidopsis, are crucial for meiotic recombination. ASY1, as other HORMADs, is assembled on the axis at early meiosis and depleted when homologous chromosomes synapse. Puzzlingly, both processes are catalyzed by AAA+ ATPase PCH2 together with its cofactor COMET. Here, we show that the ASY1 remodeling complex is temporally and spatially differently assembled. While PCH2 and COMET appear to directly interact in the cytoplasm in early meiosis, PCH2 is recruited by the transverse filament protein ZYP1 and brought to the ASY1-bound COMET assuring the timely removal of ASY1 during chromosome synapsis. Since we found that the PCH2 homolog TRIP13 also binds to the ZYP1 homolog SYCP1 in mouse, we postulate that this mechanism is conserved among eukaryotes. Deleting the PCH2 binding site of ZYP1 led to a failure of ASY1 removal. Interestingly, the placement of one obligatory crossover per homologous chromosome pair, compromised by ZYP1 depletion, is largely restored in this separation-of-function zyp1 allele suggesting that crossover assurance is promoted by synapsis. In contrast, this zyp1 allele, similar to the zyp1 null mutant, showed elevated type I crossover numbers indicating that PCH2-mediated eviction of ASY1 from the axis restricts crossover formation.

Identifiants

pubmed: 36504011
pii: 6887606
doi: 10.1093/nar/gkac1160
pmc: PMC9825157
doi:

Substances chimiques

Adenosine Triphosphatases EC 3.6.1.-
Arabidopsis Proteins 0
PCH2 protein, Arabidopsis EC 3.6.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

12924-12937

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Auteurs

Chao Yang (C)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China.
Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Kostika Sofroni (K)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Yuki Hamamura (Y)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Bingyan Hu (B)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Hasibe Tunçay Elbasi (HT)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Martina Balboni (M)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Lei Chu (L)

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China.

Dagmar Stang (D)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Maren Heese (M)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

Arp Schnittger (A)

Department of Developmental Biology, Institute of Plant Science and Microbiology, University of Hamburg, Hamburg 22609, Germany.

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