Incomplete Synapsis and Chiasma Localization: The Chicken or the Egg?

Viera, Alberto; Santos, Juan Luis; Parra, María Teresa; Calvente, Adela; Gómez, R.; Fuente, Roberto de la; Suja, José Á.; Page, Jesús; Vega, Carlos García de la; Rufas, Julio S.

doi:10.1159/000290637

Cited by 8 publications

(8 citation statements)

References 114 publications

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“…Indeed, we previously reported that partial synapsis occurs but overall synapsis was strongly affected in axr1 -/-. Localized chiasma in restricted regions of some chromosomes that undergo pairing were also reported in various fungi, animals and plants [47,48] but these were rarely associated with CO clustering. Only the Arabidopsis pss1 and the Sordaria mer2-17 show such a phenotype, but to a lesser extent and with a less pronounced synapsis defect than in axr1 -/- [28,49].…”

Section: Discussionmentioning

confidence: 80%

AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization

et al. 2020

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Meiotic crossovers (COs) are important for reshuffling genetic information between homologous chromosomes and they are essential for their correct segregation. COs are unevenly distributed along chromosomes and the underlying mechanisms controlling CO localization are not well understood. We previously showed that meiotic COs are mis-localized in the absence of AXR1, an enzyme involved in the neddylation/rubylation protein modification pathway in Arabidopsis thaliana. Here, we report that in axr1-/-, male meiocytes show a strong defect in chromosome pairing whereas the formation of the telomere bouquet is not affected. COs are also redistributed towards subtelomeric chromosomal ends where they frequently form clusters, in contrast to large central regions depleted in recombination. The CO suppressed regions correlate with DNA hypermethylation of transposable elements (TEs) in the CHH context in axr1-/meiocytes. Through examining somatic methylomes, we found axr1-/affects DNA methylation in a plant, causing hypermethylation in all sequence contexts (CG, CHG and CHH) in TEs. Impairment of the main pathways involved in DNA methylation is epistatic over axr1-/for DNA methylation in somatic cells but does not restore regular chromosome segregation during meiosis. Collectively, our findings reveal that the neddylation pathway not only regulates hormonal perception and CO distribution but is also, directly or indirectly, a major limiting pathway of TE DNA methylation in somatic cells.

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Section: Discussionmentioning

confidence: 80%

AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization

et al. 2020

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“…In mammals, this damage is typically signalled by the phosphorylation of histone variant H2AX (γH2AX), which rapidly expands to large regions of the nucleus (Mahadevaiah et al, 2001 ). Likewise, the onset of meiosis in grasshoppers is characterised by the presence of high levels of γH2AX, although with a much reduced number of RAD51 foci if compared to that found in mammals (Calvente et al, 2005 ;Viera et al, 2004a;Viera et al, 2009b ;Viera et al, 2010 ). In both cases, DNA repair may be related to the reduction or absence of transcription observed in leptotene.…”

Section: Figmentioning

confidence: 99%

Transcription reactivation during the first meiotic prophase in bugs is not dependent on synapsis

et al. 2016

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During meiosis, transcription is precisely regulated in relation to the process of chromosome synapsis. In mammals, transcription is very low until the completion of synapsis in early pachytene, and then reactivates during mid pachytene, up to the end of diplotene. Moreover, chromosomes or chromosomal regions that do not achieve synapsis undergo a specific process of inactivation called meiotic silencing of unpaired chromatin (MSUC). Sex chromosomes, which are mostly unsynapsed, present a special case of inactivation named meiotic sex chromosome inactivation (MSCI). Although processes that are similar to MSUC/MSCI have been described in other species like Sordaria and Caenorhabditis elegans, very few studies have been developed in insects. We present a study on the relationships between synapsis and transcription in two hemipteran species (Graphosoma italicum and Carpocoris fuscispinus) that possess holocentric chromosomes but develop different synaptic patterns. We have found that transcription, revealed by the presence of RNA polymerase II, is very low at the beginning of meiosis, but robustly increases during zygotene, long before the completion of synapsis, excepting in the sex chromosomes. In fact, we show that histone H3 methylation at lysine 9 (H3K9me3) may be present in the sex chromosomes at leptotene, thus acting as a likely epigenetic mark for this inactive state. Our results suggest that the meiotic transcription in these two species is differently regulated from that of mammals and, therefore, offer new opportunities to understand the relationship between synapsis and transcription and the mechanisms that govern MSUC/MSCI processes.

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“…grossum show a remarkable nuclear polarization of the axis maturation of cohesin subunits, and the location of γ-H2AX, which marks the sites of double-strand breaks, and RAD51, which is involved in homology search. This polarization was observed in both squashed and spread spermatocytes [31, 38, 39], and is maintained throughout prophase I along the chromosome regions that either are undergoing or are about to undergo synapsis (Fig 1C–1N). The identification of different early prophase I stages was carried out according to the degree of synapsis displayed by the shortest chromosomes and the chromatin morphology.…”

Section: Resultsmentioning

confidence: 92%

“…The identification of different early prophase I stages was carried out according to the degree of synapsis displayed by the shortest chromosomes and the chromatin morphology. According to these observations, it was proposed that the restricted distribution of recombination events along the chromosomal axes is responsible for the incomplete presynaptic homologous alignment and, hence, for the partial synaptonemal complex formation displayed by most bivalents[31, 38]. This proposal did not exclude the possibility that these processes may also be influenced and modulated by changes in chromatin organization.…”

Section: Resultsmentioning

confidence: 99%

“…This peculiar nuclear chromosome disposition and, likely, the chromatin organization in unsynapsed chromosome regions are factors that could be involved in the strict localization of the single chiasma at the pericentromeric regions of L1-M8 bivalents [38, 39]. Despite the high increase of exogenous DNA DSBs originated by irradiation, cytologically manifested by the γ-H2AX distribution in the whole nuclei, only 13% of the metaphase I bivalents analyzed (30/232) showed two chiasmata (Fig 4A, 4A’, 4B, 4B’, 4E and 4F).…”

Section: Discussionmentioning

confidence: 99%

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Do Exogenous DNA Double-Strand Breaks Change Incomplete Synapsis and Chiasma Localization in the Grasshopper Stethophyma grossum?

2016

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Meiotic recombination occurs as a programmed event that initiates by the formation of DNA double-strand breaks (DSBs) that give rise to the formation of crossovers that are observed as chiasmata. Chiasmata are essential for the accurate chromosome segregation and the generation of new combinations of parental alleles. Some treatments that provoke exogenous DSBs also lead to alterations in the recombination pattern of some species in which full homologous synapsis is achieved at pachytene. We have carried out a similar approach in males of the grasshopper Stethophyma grossum, whose homologues show incomplete synapsis and proximal chiasma localization. After irradiating males with γ rays we have studied the distribution of both the histone variant γ-H2AX and the recombinase RAD51. These proteins are cytological markers of DSBs at early prophase I. We have inferred synaptonemal complex (SC) formation via identification of SMC3 and RAD 21 cohesin subunits. Whereas thick and thin SMC3 filaments would correspond to synapsed and unsynapsed regions, the presence of RAD21 is only restricted to synapsed regions. Results show that irradiated spermatocytes maintain restricted synapsis between homologues. However, the frequency and distribution of chiasmata in metaphase I bivalents is slightly changed and quadrivalents were also observed. These results could be related to the singular nuclear polarization displayed by the spermatocytes of this species.

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Incomplete Synapsis and Chiasma Localization: The Chicken or the Egg?

Cited by 8 publications

References 114 publications

AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization

AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization

Transcription reactivation during the first meiotic prophase in bugs is not dependent on synapsis

Do Exogenous DNA Double-Strand Breaks Change Incomplete Synapsis and Chiasma Localization in the Grasshopper Stethophyma grossum?

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