A spontaneous mutation in MutL‐Homolog 3 (Hv<scp>MLH</scp>3) affects synapsis and crossover resolution in the barley desynaptic mutant <i>des10</i>

Colas, Isabelle; Macaulay, Malcolm; Higgins, James D.; Phillips, Dylan; Barakate, Abdellah; Posch, Markus; Armstrong, Susan J.; Franklin, F. Chris H.; Halpin, Claire; Waugh, Robbie; Ramsay, Luke

doi:10.1111/nph.14061

Cited by 45 publications

(105 citation statements)

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“…Similarly, in des10 , discrete ASY1 foci could be detected on late diplotene chromosomes and in the cytoplasm (Figure 4g). Moreover, due to the des10 having a longer prophase (Colas et al, 2016), it was possible to see the separation of the bivalent ends (telomeric regions) resulting from a defect in chiasmata formation (Figure 4h) and detect ASY1 signal in the same region (Figure 4h, arrow). At metaphase I (Figure 4i), des10 behaved as in the wild type with no detectable ASY1 signal on the chromosomes, but a considerable amount in the cytoplasm.…”

Section: Resultsmentioning

confidence: 96%

“…To test whether a perturbed synapsis would impact on this striking distribution of ASY1 at diplotene, we then examined the barley desynapsis10 meiotic mutant ( Des10 = HvMlh3 ) in which normal synapsis and chromatin organization are (Colas et al, 2016). Early prophase I in des10 appears cytologically normal while at later stages, polymerization of ZYP1 is severely compromised (Colas et al, 2016).…”

Section: Resultsmentioning

confidence: 99%

“…Early prophase I in des10 appears cytologically normal while at later stages, polymerization of ZYP1 is severely compromised (Colas et al, 2016). Despite this obvious impediment, des10 mutants form tinsel-structures during SC dissolution (Figures 2a,b, and Supplementary Video 8), though their organization is distinct from wild type.…”

Section: Resultsmentioning

confidence: 99%

“…We have previously shown that in the barley meiotic mutant des10 , the chromatin compaction/extension cycle was perturbed (Colas et al, 2016). As a consequence, synapsis in wheat and des10 superficially appear to be similar as it was also not always possible to observe the tri-partite structure in des10 .…”

Section: Discussionmentioning

confidence: 99%

“…As a consequence, synapsis in wheat and des10 superficially appear to be similar as it was also not always possible to observe the tri-partite structure in des10 . Therefore, it is possible that the absence of obvious tri-partite structure in both wheat and des10 are due to higher chromosome coiling and chromatin compaction (Colas et al, 2016). …”

Section: Discussionmentioning

confidence: 99%

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Observation of Extensive Chromosome Axis Remodeling during the “Diffuse-Phase” of Meiosis in Large Genome Cereals

et al. 2017

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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.

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Section: Resultsmentioning

confidence: 96%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Observation of Extensive Chromosome Axis Remodeling during the “Diffuse-Phase” of Meiosis in Large Genome Cereals

et al. 2017

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Chromosome Synapsis and Recombination in Cereals

Orr

Lewandowska

Waugh

et al. 2021

Annual Plant Reviews Online

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Crops are under constant pressure due to climate change imposing dramatic changes in rainfall, temperature, and soil salinity. They are also under high stress due to pests and diseases, costing yield, and income loss to farmers. Thus, there is a need to create more resilient varieties. New favourable allelic combinations are achieved via homologous recombination during a process called meiosis. During meiosis, homologous chromosomes pair, synapse, and recombine; but crossover (CO) sites are rare, limiting the creation of valuable allelic recombinants. In large genome crops, such as barley or wheat, crossovers are not only scarce (2 or 3 per chromosome), they are also mainly located at the ends of the chromosomes, leaving 20–30% of genes in the pericentromeric region which breeding cannot exploit (https://youtu.be/XyMhyeWMZl4). The use of downregulated lines for specific meiotic gene candidates (e.g. RECQ4) has shown successful and promising translational research from the model plantArabidopsis thalianato crops, raising hopes for using this approach in breeding programs. The development of new tools, technologies, and protocols have demonstrated new insights into the progression of meiosis crops – highlighting unique meiotic phenomena not observed inArabidopsis– and revealed a higher cost of meiotic mutants on fertility than previously thought suggesting a more intricate relationship between meiotic events. In this article, we have selected a number of studies to show the relationship between synaptonemal complex formation and the recombination machinery.

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Preparation of Barley Pollen Mother Cells for Confocal and Super Resolution Microscopy

Mittmann

Arrieta

Ramsay

et al. 2018

Methods in Molecular Biology

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Recombination (crossing over) drives the release of genetic diversity in plant breeding programs. However, in barley, recombination is skewed towards the telomeric ends of its seven chromosomes, restricting the re-assortment of about 30% of the genes located in the centromeric regions of its large 5.1 Gb genome. A better understanding of meiosis and recombination could provide ways of modulating crossover distribution and frequency in barley as well as in other grasses, including wheat. While most research on recombination has been carried out in the model plant Arabidopsis thaliana, recent studies in barley have provided new insights into the control of crossing over in large genome species. A major achievement in these studies has been the use of cytological procedures to follow meiotic events. This protocol provides detailed practical steps required to perform immunostaining of barley meiocytes (developing pollen) for confocal or structured illumination microscopy.

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A spontaneous mutation in MutL‐Homolog 3 (HvMLH3) affects synapsis and crossover resolution in the barley desynaptic mutant des10

Cited by 45 publications

References 77 publications

Observation of Extensive Chromosome Axis Remodeling during the “Diffuse-Phase” of Meiosis in Large Genome Cereals

Observation of Extensive Chromosome Axis Remodeling during the “Diffuse-Phase” of Meiosis in Large Genome Cereals

Chromosome Synapsis and Recombination in Cereals

Preparation of Barley Pollen Mother Cells for Confocal and Super Resolution Microscopy

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