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Comparative Study
. 2021 Mar 12;22(1):181.
doi: 10.1186/s12864-021-07497-2.

Comparative transcriptomic analysis of thermally stressed Arabidopsis thaliana meiotic recombination mutants

Jiyue Huang #  1 , Hongkuan Wang #  2 , Yingxiang Wang  3 , Gregory P Copenhaver  4   5
Affiliations
Comparative Study

Comparative transcriptomic analysis of thermally stressed Arabidopsis thaliana meiotic recombination mutants

Jiyue Huang et al. BMC Genomics. .

Abstract

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. In addition, SDS the meiosis-specific cyclin-like gene, DMC1 the meiosis-specific recombinase, SYN1/REC8 the meiosis-specific cohesion complex component, and SWI1 which functions in meiotic sister chromatid cohesion are up-regulated in all three genotypes. 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.

Keywords: ASY1; Heat stress; MSH4; MUS81; Meiotic recombination; RNA-Seq.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Characteristics of the heat-stressed and control transcriptomes in WT, mus81 and msh4. a. The number of expressed genes in the six experimental samples. b. Gene expression value in all samples with two biological replicates (**P value < 2.2e-16 from Mann–Whitney test). c. Expressed genes grouped from low to high from all the six experimental samples
Fig. 2
Fig. 2
Characteristics of the differentially expressed genes (DEGs) from WT, mus81 and msh4 Arabidopsis grown under 20 °C and 28 °C conditions. a. Venn diagram showing the common and specific up-regulated DEGs under heat stress among WT, mus81 and msh4. b. Venn diagram showing the common and specific down-regulated DEGs under heat stress among WT, mus81 and msh4. c. Expression of ASY1 from WT, mus81 and msh4 grown under 20 °C and 28 °C conditions. d. Snapshot showing that ASY1 is an up-regulated DEG in WT and mus81 but not in msh4
Fig. 3
Fig. 3
GO analysis of DEGs from WT, mus81 and msh4. a. GO analysis of biological processes of up-regulated DEGs from WT, mus81 and msh4. b. GO analysis of molecular functions of up-regulated DEGs from WT and mus81. Results in (a and b) were simplified by removing redundant GO terms, for full lists please see Supplementary Data 1. c. GO analysis of cellular components of up-regulated DEGs from WT and mus81. d. GO analysis of biological processes enriched in the 278 up-regulated DEGs shared by WT and mus81
Fig. 4
Fig. 4
Genome-wide distribution of up- and down-regulated DEGs from WT, mus81 and msh4 along the Arabidopsis chromosomes. a. Density plot of up-regulated DEGs from WT, mus81 and msh4 along the Arabidopsis chromosomes with the distribution of expressed genes in WT as a control. b. Local enrichment analysis of up-regulated DEGs from mus81 and msh4. c. Density plot of down-regulated DEGs from WT, mus81 and msh4 along the Arabidopsis chromosomes with the distribution of expressed genes in WT as a control. d. Local enrichment analysis of down-regulated DEGs from mus81 and msh4. Chromosomes are partitioned into arm regions and centromeric regions (blue dashed lines) in (a, b, c and d). The horizontal black dashed lines in b and d indicate the P value = 0.05 from fisher test. Arrows in d show the two segments where there are significantly more down-regulated DEGs in msh4 than in WT.
Fig. 5
Fig. 5
Heatmap of gene expression data from 148 gene with previously defined meiotic functions from WT, mus81 and msh4 plants grown at 20 °C and 28 °C. The ranges of colors in the heatmap represent lower (white) to higher (dark red) relative expression of each gene (rows) in each sample (columns)
Fig. 6
Fig. 6
Characteristics of novel transcripts from anther derived samples. a Novel transcripts grouped from low to high from all the six experimental samples. b Comparison of transcript length from 51 novel transcripts and 38,194 annotated genes (**P value < 2.2e-16 from Mann–Whitney test). c Comparison of exon number per transcript from 51 novel transcripts and 38,194 annotated genes. d Venn diagram showing the common and specific differential expressed novel transcripts under heat stress among WT, mus81 and msh4. e Density plot of 51 novel transcripts along the Arabidopsis chromosomes with the distribution of expressed genes in WT as a control. Numbers in yellow indicate the positions of the 19 anther-specific novel transcripts (1 novel transcript localizes in the Mitochondrial DNA). f An A-rich motif is enriched in putative promoter sequences of the 51 novel transcripts. g Snapshot showing the anther-specific novel transcript MSTRG.16271
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