Heat stress interferes with chromosome segregation and cytokinesis during male meiosis in<i>Arabidopsis thaliana</i>

Lei, Xiaoning; Ning, Yingjie; Elesawi, Ibrahim Eid; Yang, Ke; Chen, Chunli; Wang, Chong; Liu, Bing

doi:10.1080/15592324.2020.1746985

Cited by 29 publications

(40 citation statements)

References 61 publications

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“…Orcein staining of meiotic products was performed by referring to (Lei et al, 2020). For the quantification of fluorescent foci of γH2A.X and DMC1, we referred to (Xue et al, 2018;Yao et al, 2020).…”

Section: Cytology and Quantification Of γH2ax And Dmc1 Focimentioning

confidence: 99%

“…Goat anti-Rabbit IgG (H+L) Cross-Adsorbed Secondary Antibody Alexa Fluor 555 (Invitrogen, A32732) and Goat anti-Rabbit IgG (H+L) Highly Cross-Adsorbed Secondary Antibody Alexa Fluor Plus 488 (Invitrogen, A32731) were diluted by 1:400. FISH and used centromere-specific probes were referred to (Lei et al, 2020).…”

Section: Immunolocalization and Fluorescence In Situ Hybridization (Fmentioning

confidence: 99%

“…Environmental temperatures can affect multiple processes of meiotic cell division in plants (Liu et al, 2019;Morgan et al, 2017). In Arabidopsis, wheat, Populus and persimmon, temperature stresses affect formation and organization of spindle and/or phragmoplast during male meiosis, which results in meiotic restitution or aneuploid gametes (De Storme et al, 2012;Lei et al, 2020;Liu et al, 2018;Mai et al, 2019;Tang et al, 2011;Wang et al, 2017). In the context of MR, both decrease and increase of temperature within fertility threshold (8-28°C) promotes MR rate via enhanced type-I CO formation in Arabidopsis (Francis et al, 2007;Lloyd et al, 2018;Modliszewski et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Cytology and Quantification Of γH2ax And Dmc1 Focimentioning

confidence: 99%

Section: Immunolocalization and Fluorescence In Situ Hybridization (Fmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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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“…In both dicots and monocots, low temperatures predominantly affect cytokinesis by disturbing the formation of phragmoplast, which thereby induces meiotic restitution and formation of unreduced gametes (De Storme et al, 2012; Liu et al, 2018; Tang et al, 2011). In contrast, under high temperatures, both chromosome dynamics and cytokinesis are prone to be impacted; especially, the response of MR to heat stress is more complex (De Storme and Geelen, 2020; Draeger and Moore, 2017; Lei et al, 2020; Mai et al, 2019; Ning et al, 2021; Wang et al, 2017). In Arabidopsis, a mild increase of temperature (28°C) positively affects type-I CO rate by enhancing the activity of ZMM proteins without impacting DSB formation (Lloyd et al, 2018; Modliszewski et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Mechanistic Insights of High Temperature-Interfered Meiosis in Autotetraploid Arabidopsis thaliana

Yang

Zhang

et al. 2021

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Environmental temperature has a huge impact on multiple meiosis processes in flowering plants. Polyploid plants derived from whole genome duplication are believed to have an enhanced abiotic stress tolerance. In this study, the impact of high temperatures on male meiosis in autotetraploid Arabidopsis thaliana was investigated. We found that autotetraploid Columbia (Col-0) plants generate a subpopulation of aberrant meiotic products under normal temperature, which is significantly increased under heat stress. Cytological studies revealed that, as the case in diploid Arabidopsis thaliana, assembly of microtubular cytoskeleton network, pairing and segregation of homologous chromosomes, and meiotic recombination in autotetraploid Arabidopsis are compromised under the high temperatures. Immunostaining of ?H2A.X and recombinase DMC1 suggested that heat stress inhibits formation of DNA double-strand breaks; additionally, it specifically destabilizes ASY1 and ASY4, but not SYN1 on chromosomes. The loading defects of ASY1 and ASY4 overlap in the syn1 mutant, which supports that the building of lateral element of synaptonemal complex occurs downstream of a SYN1-ASY4-ASY3 stepwise assembly of axis. Remarkably, heat-induced abnormalities of ASY1 and ASY4 co-localize on chromosomes of both diploid and autotetraploid Arabidopsis, suggesting that high temperatures interfere with ASY1-associated SC via an impacted stability of chromosome axis. Furthermore, ZYP1-dependent transverse filament of SC is disrupted by heat stress. Taken together, these findings suggest that polyploidization negatively contributes to instability of chromosomes and meiotic recombination in Arabidopsis thaliana under heat stress.

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“…In Hordeum vulgare (barley), a shift from 15 °C to 30 °C resulted in an incremental increase in male (but not female) CO frequencies, but also a distinct shift from proximal to distal COs along the chromosome arms [7]. At even higher temperatures, meiotic mechanisms begin to fail resulting in infertility [8,9].…”

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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Heat stress interferes with chromosome segregation and cytokinesis during male meiosis inArabidopsis thaliana

Cited by 29 publications

References 61 publications

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

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

Mechanistic Insights of High Temperature-Interfered Meiosis in Autotetraploid Arabidopsis thaliana

Comparative Transcriptomic Analysis of Thermally Stressed Arabidopsis thaliana Meiotic Recombination Mutants

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