Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis

PLoS Genet. 2020 Apr 20;16(4):e1007881. doi: 10.1371/journal.pgen.1007881. eCollection 2020 Apr.

Abstract

Meiotic double-strand breaks (DSBs) are generated by the evolutionarily conserved SPO11 complex in the context of chromatin loops that are organized along axial elements (AEs) of chromosomes. However, how DSBs are formed with respect to chromosome axes and the SPO11 complex remains unclear in plants. Here, we confirm that DSB and bivalent formation are defective in maize spo11-1 mutants. Super-resolution microscopy demonstrates dynamic localization of SPO11-1 during recombination initiation, with variable numbers of SPO11-1 foci being distributed in nuclei but similar numbers of SPO11-1 foci being found on AEs. Notably, cytological analysis of spo11-1 meiocytes revealed an aberrant AE structure. At leptotene, AEs of wild-type and spo11-1 meiocytes were similarly curly and discontinuous. However, during early zygotene, wild-type AEs become uniform and exhibit shortened axes, whereas the elongated and curly AEs persisted in spo11-1 mutants, suggesting that loss of SPO11-1 compromised AE structural maturation. Our results reveal an interesting relationship between SPO11-1 loading onto AEs and the conformational remodeling of AEs during recombination initiation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Chromosome Pairing
  • DNA Breaks, Double-Stranded
  • Endodeoxyribonucleases / genetics
  • Endodeoxyribonucleases / metabolism*
  • Genes, Plant / genetics
  • Homologous Recombination*
  • Meiosis* / genetics
  • Mutation
  • Phenotype
  • Zea mays / cytology*
  • Zea mays / genetics
  • Zea mays / metabolism*

Substances

  • Endodeoxyribonucleases
  • meiotic recombination protein SPO11

Grants and funding

This work was funded by a grant no. GM48547 from the National Institutes of Health (https://www.nih.gov/) to WZC, a research grant no. PAPIIT IA201217 from the National Autonomous University of Mexico (https://www.unam.mx/) to AR, a research grant IOS-1339130 from the US National Science Foundation (https://www.nsf.gov/) to AB, and research grants no. 107-2923-B-002-001-MY4 and 103-2311-B-001-014 from the Taiwan Ministry of Science and Technology (https://www.most.gov.tw) to CJRW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.