High temperatures alter cross-over distribution and induce male meiotic restitution in Arabidopsis thaliana

Storme, Nico De; Geelen, Danny

doi:10.1038/s42003-020-0897-1

Cited by 73 publications

(87 citation statements)

References 48 publications

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“…To investigate the effect of zyp1 on the Class I interference-sensitive CO pathway, HEI10 foci numbers were compared between the mutant and wild type ( 56 ). HEI10 is the A. thaliana ortholog of S. cerevisiae Zip3 and promotes formation of Class I COs ( 57 ). In the wild type, as previously reported, a large number of foci were observed at late zygotene/early pachytene (

= 44.7, SD = 18.7, n = 14) ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Studies in C. elegans suggest that the SC TF proteins limit COs and attenuate CO interference ( 40 ). However, studies in S. macrospora indicate that interference acts on a large number of recombination initiation events (∼80) giving rise to a smaller number (∼45 to 50) of patterned, evenly spaced, synapsis initiation sites and CO designations, thereby arguing that CO patterning is established prior to SC formation ( 35 , 57 ). Studies in S. cerevisiae also support a model of early CO designation ( 6 , 32 , 59 ).…”

Section: Discussionmentioning

confidence: 99%

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ZYP1 is required for obligate cross-over formation and cross-over interference inArabidopsis

Enderle

Röhrig

Puchta

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

132

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The synaptonemal complex is a tripartite proteinaceous ultrastructure that forms between homologous chromosomes during prophase I of meiosis in the majority of eukaryotes. It is characterized by the coordinated installation of transverse filament proteins between two lateral elements and is required for wild-type levels of crossing over and meiotic progression. We have generated null mutants of the duplicated Arabidopsis transverse filament genes zyp1a and zyp1b using a combination of T-DNA insertional mutants and targeted CRISPR/Cas mutagenesis. Cytological and genetic analysis of the zyp1 null mutants reveals loss of the obligate chiasma, an increase in recombination map length by 1.3- to 1.7-fold and a virtual absence of cross-over (CO) interference, determined by a significant increase in the number of double COs. At diplotene, the numbers of HEI10 foci, a marker for Class I interference-sensitive COs, are twofold greater in the zyp1 mutant compared to wild type. The increase in recombination in zyp1 does not appear to be due to the Class II interference-insensitive COs as chiasmata were reduced by ∼52% in msh5/zyp1 compared to msh5. These data suggest that ZYP1 limits the formation of closely spaced Class I COs in Arabidopsis. Our data indicate that installation of ZYP1 occurs at ASY1-labeled axial bridges and that loss of the protein disrupts progressive coalignment of the chromosome axes.

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= 44.7, SD = 18.7, n = 14) ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

ZYP1 is required for obligate cross-over formation and cross-over interference inArabidopsis

Enderle

Röhrig

Puchta

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

132

View full text Add to dashboard Cite

show abstract

“…A recent study in Arabidopsis have revealed that at 32°C, ASY1 foci appear normal but linear configuration of ZYP1 on pachytene chromosomes is interrupted (De Storme and Geelen, 2020). In barley, a moderate high temperature causes a slight but significant decrease of CO formation by affecting ZYP1-dependent SC assembly (Higgins et al, 2012).…”

Section: Chromosome Axis and Sc Assembly Are Prominent Targets Of Higmentioning

confidence: 98%

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Ning

Liu

Wang

et al. 2020

Preprint

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Meiotic recombination (MR) drives reciprocal exchange of genetic information which allows novel combination of alleles and contributes to genomic diversity of eukaryotes. In this study, we report that heat stress (36-38°C) over fertile threshold fully abolishes crossover occurrence by lowering the formation of SPO11-dependent double-strand breaks (DSBs) in Arabidopsis. The high temperature partially suppresses chromosome fragmentation in the rad51 and syn1 mutants by reducing DSB formation. In addition, we found that although the SYN1-mediated formation of chromosome axis is not influenced by the high temperature, ASY1-associated axial element of synaptonemal complex (SC) is partially compromised, and the ZYP1-dependent central element of axis is severely disrupted, indicating that homology synapsis is another prominent target of high temperature. Besides, we observed that the loading of recombinase DMC1 on chromatin is significantly reduced by high temperatures, suggesting that heat stress interferes with DMC1-dependent MR. Moreover, we found that the numbers of DSB and DMC1 keep stable within a limited range of temperature increase, while decrease when the DSB-processing system reaches threshold to heat. Furthermore, transcriptome study revealed a universal variation of the expression of meiotic genes under low (4°C) and high (32°C) temperatures, suggesting that temperature may influence MR by modulating the transcription of MR-related factors. We also found that the landscape of 5-methylcytosine (5mC) was altered under high temperatures, suggesting that environmental temperature may influence the distribution of MR via reshaped DNA methylation status of chromatin. Taken together, our findings provide evidence shedding light on how environment temperatures influence MR in Arabidopsis.

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“…These results are consistent with the hypothesis that the regulation of ASY1 gene expression in uences meiotic recombination levels. However, recent studies in Arabidopsis reported no change in ASY1 immunostaining in wild type meiocytes after 30-32 °C heat shock for 24 hours [4], but partially compromised localization under 36-38 °C extreme heat stress conditions [31]. It is important to note that the regulatory responses to moderate environmental stresses may not be re ected in more extreme conditions which can instead result in meiotic failure.…”

Section: Discussionmentioning

confidence: 96%

“…In the absence of a CO, chromosomes segregate randomly, resulting in chromosome number imbalances, or aneuploidy, in the gametes which, in turn, can result in developmental defects or lethality in progeny. Regulation of the frequency and distribution of COs in the genome has been studied extensively [1] and more recently, advances have been made in our understanding of how environmental conditions and stressors in uence those regulatory mechanisms [2][3][4].…”

Section: Introductionmentioning

confidence: 99%

Comparative Transcriptomic Analysis of Thermally Stressed Arabidopsis thaliana Meiotic Recombination Mutants

Huang

Wang

et al. 2020

Preprint

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Background: Meiosis is a specialized cell division that underpins sexual reproduction in most eukaryotes. During meiosis, interhomolog meiotic recombination facilitates accurate chromosome segregation and generates genetic diversity by shuffling parental alleles in the gametes. The frequency of meiotic recombination in Arabidopsis has a U-shaped curve in response to environmental temperature, and is dependent on the Type I, crossover (CO) interference-sensitive pathway. The mechanisms that modulate recombination frequency in response to temperature are not yet known. Results: In this study, we compare the transcriptomes of thermally-stressed meiotic-stage anthers from msh4 and mus81 mutants that mediate the Type I and Type II meiotic recombination pathways, respectively. We show that heat stress reduces the number of expressed genes regardless of genotype. In addition, msh4 mutants have a distinct gene expression pattern compared to mus81 and wild type controls. Interestingly, ASY1, which encodes a HORMA domain protein that is a component of meiotic chromosome axes, is up-regulated in wild type and mus81 but not in msh4. We also characterize 51 novel, previously unannotated transcripts, and show that their promoter regions are associated with A-rich meiotic recombination hotspot motifs. Conclusions: Our transcriptomic analysis of msh4 and mus81 mutants enhances our understanding of how the Type I and Type II meiotic CO pathway respond to environmental temperature stress and might provide a strategy to manipulate recombination levels in plants.

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High temperatures alter cross-over distribution and induce male meiotic restitution in Arabidopsis thaliana

Cited by 73 publications

References 48 publications

ZYP1 is required for obligate cross-over formation and cross-over interference inArabidopsis

ZYP1 is required for obligate cross-over formation and cross-over interference inArabidopsis

Heat Stress Interferes with Formation of Double-Strand Breaks and Homolog Synapsis inArabidopsis thaliana

Comparative Transcriptomic Analysis of Thermally Stressed Arabidopsis thaliana Meiotic Recombination Mutants

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