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

Sepsi et al. Centromeres and pairing at meiosis in wheat

Sepsi, Higgins, Heslop-Harrison and Schwarzacher. 2016. Centromeres and progression of chromosome pairing at meiosis in wheat. Plant Journal

330. Sepsi A, Higgins JD, Heslop-Harrison JS, Schwarzacher T. 2017. CENH3 morphogenesis reveals dynamic centromere associations during synaptonemal complex formation and the progression through male meiosis in hexaploid wheat. Plant Journal 89: 235-249. http://dx.doi.org/10.1111/tpj.13379 and Author Version: Sepsi et al. 2016. CENH3 and wheat meiosis. Plant Journal. See bottom of page for YouTube video links.

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.

SIGNIFICANCE STATEMENT
During meiosis, centromeres in some species undergo a series of associations, but the role of these associations to subsequent chromosome pairing is still debated. Here, we used
immunolocalization of centromere and synaptonemal complex proteins to correlate meiotic centromere dynamics and early telomere behaviour to the progression of chromosome pairing in wheat. We found that centromere clusters gradually resolve after subtelomeric synapsis, and that this centromere depolarisation and individualization precedes elongation of interstitial arm synapsis.
KEY WORDS
Triticum aestivum L., CENH3, Meiosis, Synaptonemal complex, ASY1, ZYP1, centromere
associations, centromere pairing, chromatin expansion-contraction

Sepsi A, Higgins JD, Heslop-Harrison JS, Schwarzacher T. 2016. CENH3 morphogenesis reveals dynamic centromere associations during synaptonemal complex formation and the progression through male meiosis in hexaploid wheat. Plant Journal 89: 235-249. http://dx.doi.org/10.1111/tpj.13379 and Author Version: Sepsi et al. 2016. CENH3 and wheat meiosis. Plant Journal. See bottom of page for YouTube video links.

Videos showing centromere, DNA and axis locations (note some may appear black at start and end):

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About Pat Heslop-Harrison

Professor of Molecular Cytogenetics and Cell Biology, University of Leicester Chief Editor, Annals of Botany. Research: genome evolution, breeding and biodiversity in agricultural species; the impact of agriculture; evalutation of research and advanced training.
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