Differentiated function and localisation of SPO11-1 and PRD3 on the chromosome axis during meiotic DSB formation in Arabidopsis thaliana

A - Papers appearing in refereed journals

Lambing, C., Kuo, P., Kim, J., Osman, K., Whitbread, A. L., Yang, J., Choi, K., Franklin, F. C. H. and Henderson, I. R. 2022. Differentiated function and localisation of SPO11-1 and PRD3 on the chromosome axis during meiotic DSB formation in Arabidopsis thaliana. PLOS Genetics. 18 (7), p. e1010298. https://doi.org/10.1371/journal.pgen.1010298

AuthorsLambing, C., Kuo, P., Kim, J., Osman, K., Whitbread, A. L., Yang, J., Choi, K., Franklin, F. C. H. and Henderson, I. R.
Abstract

During meiosis, DNA double-strand breaks (DSBs) occur throughout the genome, a subset of which are repaired to form reciprocal crossovers between chromosomes. Crossovers are essential to ensure balanced chromosome segregation and to create new combinations of genetic variation. Meiotic DSBs are formed by a topoisomerase-VI-like complex, containing catalytic (e.g. SPO11) proteins and auxiliary (e.g. PRD3) proteins. Meiotic DSBs are formed in chromatin loops tethered to a linear chromosome axis, but the interrelationship between DSB-promoting factors and the axis is not fully understood. Here, we study the localisation of SPO11-1 and PRD3 during meiosis, and investigate their respective functions in relation to the chromosome axis. Using immunocytogenetics, we observed that the localisation of SPO11-1 overlaps relatively weakly with the chromosome axis and RAD51, a marker of mei- otic DSBs, and that SPO11-1 recruitment to chromatin is genetically independent of the axis. In contrast, PRD3 localisation correlates more strongly with RAD51 and the chromo- some axis. This indicates that PRD3 likely forms a functional link between SPO11-1 and the chromosome axis to promote meiotic DSB formation. We also uncovered a new function of SPO11-1 in the nucleation of the synaptonemal complex protein ZYP1. We demonstrate that chromosome co-alignment associated with ZYP1 deposition can occur in the absence of DSBs, and is dependent on SPO11-1, but not PRD3. Lastly, we show that the progression of meiosis is influenced by the presence of aberrant chromosomal connections, but not by the absence of DSBs or synapsis. Altogether, our study provides mechanistic insights into the control of meiotic DSB formation and reveals diverse functional interactions between SPO11-1, PRD3 and the chromosome axis.

Year of Publication2022
JournalPLOS Genetics
Journal citation18 (7), p. e1010298
Digital Object Identifier (DOI)https://doi.org/10.1371/journal.pgen.1010298
Web address (URL)https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1010298
Open accessPublished as ‘gold’ (paid) open access
FunderBiotechnology and Biological Sciences Research Council
Global Challenges Research Fund (UKRI)
Funder project or codeDesigning Future Wheat (DFW) [ISPG]
21ROMITIGATIONFUND
Publisher's version
Output statusPublished
Publication dates
Online20 Jul 2022
Publication process dates
Accepted16 Jun 2022
PublisherPublic Library of Science (PLOS)
ISSN1553-7404

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