Abstract
The production of balanced fertile haploid gametes requires the faithful separation of paired (synapsed) chromosomes toward the end of meiotic prophase I (desynapsis). This involves the timely dissolution of the synaptonemal complex during the pachytene-diplotene transition, a stage traditionally referred to as the “diffuse stage.” In species with large genomes such as, barley (Hordeum vulgare L.) and wheat (Triticum aestivum L.) we know most about the early stages of meiotic prophase I. There, synapsis initiates at the telomeric ends of chromosomes and progresses toward the centromeric regions through the ordered assembly of the synaptonemal complex (SC). Synapsis is impacted by recombination (crossing over, CO) which locally modifies the extent of chromatin compaction and extension. CO is uneven along the chromosomes, occurring mainly toward the telomeric regions resulting in a highly skewed distribution of recombination events. However, we know very little about the process of desynapsis which occurs during the “diffuse stage,” where the synapsed and recombined chromosomes faithfully desynapse and separate into daughter cells. Here, using 3D-SIM super-resolution immuno-cytology combined with the use of antibodies directed against two crucial SC proteins, ASY1 and ZYP1, we followed the whole of meiosis I (i.e., both synapsis and desynapsis) in both barley and wheat. We showed that synapsis forms a characteristic tri-partite SC structure in zygotene (more clearly seen in barley). Toward the end of meiosis I, as the SC starts to disassemble, we show that extensive chromosome axis remodeling results in the formation of characteristic “tinsel-like” structures in both wheat and barley. By using a mutant (des10) that is severely compromised in polymerization of ZYP1during synapsis, we show that tinsel structure formation during SC dissolution is not dependant on full synapsis and may relate instead to changes in expansion stress. Our observations highlight a potentially new role for ASYNAPSIS1 (ASY1) in desynapsis, in addition to chromosome synapsis and cohesion.
Highlights
Meiosis is a pair of specialized cell divisions that are required for the formation of parental gametes prior to fertilization (Zickler and Kleckner, 1999; Zamariola et al, 2014)
In barley and wheat the chromosomes are fully synapsed and coiled (Figures 1iic,g, Supplementary Figure 3, and Supplementary Videos 4, 5) and we noted bright ASYNAPTIC 1 (ASY1) signals on the surface of the synaptonemal complex (SC) (Figures 1iic,g arrow) that potentially represents the first step in chromosome condensation and desynapsis
We conclude that desynapsis is highly coordinated in the large genome cereals barley and wheat, and involves the formation of novel “tinsel-like” structures in which ASY1 appears to play a major role
Summary
Meiosis is a pair of specialized cell divisions (meiosis I and II) that are required for the formation of parental gametes prior to fertilization (Zickler and Kleckner, 1999; Zamariola et al, 2014). Prior to the formation of the SC, proteins such as, ASYNAPTIC 1 (ASY1) organize the chromosome axes by interacting with chromatin to form lateral elements as early as leptotene. Toward the end of meiosis I, homologous chromosomes that are paired all along their length subsequently need to separate and divide faithfully into daughter cells. This occurs by dissolution of the SC, during the transition from pachytene to diplotene (that includes the cytologically defined “diffuse stage”) with the sites of CO physically holding homolog together and orienting chromosomes prior to division (Zickler and Kleckner, 1998, 1999; Zickler, 2006; Mercier et al, 2014). Aberrations in SC dissolution are deleterious and can lead to chromosome mis-segregation and loss of the genetic integrity (Sanchez-Moran et al, 2007; Joyce and McKim, 2010; Kim et al, 2014)
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