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CENH3 morphogenesis reveals dynamic centromere associations during synaptonemal complex formation and the progression through male meiosis in hexaploid wheat.

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posted on 2016-11-23, 17:45 authored by Adel Sepsi, James D. Higgins, J.S. Pat Heslop-Harrison, Trude Schwarzacher
During meiosis, centromeres in some species undergo a series of associations, but the processes and progression to homologous pairing is still a matter of debate. Here, we aimed to correlate meiotic centromere dynamics and early telomere behaviour to the progression of synapotonemal complex (SC) construction in hexaploid wheat (2n=42) by triple immunolabelling of CENH3 protein marking functional centromeres, and SC proteins ASY1 (unpaired lateral elements) and ZYP1 (central elements in synapsed chromosomes). We show that single or multiple centromere associations formed in meiotic interphase undergo a progressive polarisation (clustering) at the nuclear periphery in early leptotene, leading to formation of the telomere bouquet. Critically, immunolabelling shows the dynamics of these presynaptic centromere associations and a structural reorganisation of the centromeric chromatin coinciding with key events of synapsis initiation from the subtelomeric regions. As short stretches of subtelomeric synapsis emerged at early zygotene, centromere clusters lost their strong polarization, gradually resolving as individual centromeres indicated by more than 21 CENH3 foci associated with unpaired lateral elements. Only following this centromere depolarisation were homologous chromosome arms connected, as observed by the alignment and fusion of interstitial ZYP1 loci elongating at zygotene so synapsis at centromeres is a continuation of the interstitial synapsis. Our results thus reveal that centromere associations are a component of the timing and progression of chromosome synapsis, and the gradual release of the individual centromeres from the clusters correlates with the elongation of interstitial synapsis between the corresponding homologues.

Funding

The research leading to these results has received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA grant agreement no 625835. We thank the Advanced Imaging Facility at the University of Leicester (Dr. Kees Straatman) for training with confocal microscopy and subsequent image analysis.

History

Citation

Plant Journal, 2016

Author affiliation

/Organisation/COLLEGE OF MEDICINE, BIOLOGICAL SCIENCES AND PSYCHOLOGY/MBSP Non-Medical Departments/Department of Genetics

Version

  • AM (Accepted Manuscript)

Published in

Plant Journal

Publisher

Wiley, Society for Experimental Biology (SEB)

issn

0960-7412

eissn

1365-313X

Acceptance date

2016-09-08

Available date

2017-09-14

Publisher version

http://onlinelibrary.wiley.com/doi/10.1111/tpj.13379/abstract

Notes

Additional Supporting Information may be found in the online version of this article.

Language

en

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