Single-base resolution methylomes of cotton CMS system reveal epigenomic changes in response to high-temperature stress during anther development

Abstract

Here, cytosine methylation at single-base resolution across the whole genome of cotton (Gossypium hirsutum L.) anthers was mapped using the whole-genome bisulfite sequencing technique, and the methylome changes associated with high-temperature (HT) stress were analysed in two cotton lines of the CMS system with contrasting HT stress tolerance. The cotton anther genome was found to display approximately 31.6%, 68.7%, 61.8%, and 21.8% methylation across all sequenced C sites and in the CG, CHG and CHH sequence contexts, respectively. In an integrated global methylome and transcriptome analysis, only promoter-unmethylated genes showed higher expression levels than promoter-methylated genes, whereas gene body methylation presented an obvious positive correlation with gene expression. The methylation profiles of transposable elements in cotton anthers were characterized, and more differentially methylated transposable elements were demethylated under HT stress. HT-induced promoter methylation changes caused upregulated expression of the mitochondrial respiratory chain enzyme-associated genes GhNDUS7, GhCOX6A, GhCX5B2, and GhATPBM, ultimately promoting a series of redox processes to form ATP for normal anther development under HT stress. In vitro application of the common DNA methylation inhibitor 5-azacytidine and accelerator methyl trifluoromethanesulfonate demonstrated that DNA demethylation promoted anther development, while increased methylation only partially inhibited anther development under HT stress.

Resistance assessment for SYP‐14288 in Phytophthora capsici and changes in mitochondria electric potential‐associated respiration and ATP production confers resistance

“…It has been reported that N6‐methyldeoxyadenine (6 mA) is a transgenerational epigenetic signal for mitochondrial stress adaptation in Caenorhabditis elegans , and Zhang et al . reported that more transposable elements were demethylated under high‐temperature stress in cotton . Combining our findings that the high‐resistance mutants against SYP‐14288 showed better adaptability at high‐temperature stress than the parental isolate (optimal growth temperatures were 30 °C for the high‐resistance mutants and 25 °C for JA8) and SYP‐14288 could induce many biochemical changes between mutants and their parental isolates, whether or not an epigenetic marker such as 6 mA was involved in SYP‐14288‐resistance in P. capsici could be further explored.…”

Integrated Methylome and Transcriptome Analysis between the CMS-D2 Line ZBA and Its Maintainer Line ZB in Upland Cotton

“…ROS homeostasis is essential for normal anther and pollen development [40,62,85], whereas excessive accumulation of ROS in anthers leads to cell apoptosis and male sterility [9,35,86,87,88]. In this study, a lower extent of H 2 O 2 production but a higher level of ATP synthesis was found in maintainer line ZB compared to ZBA (Figure 6c,d).…”

“…DNA methylation has been recognized as a new regulator of plant growth, development, and stress response [34,64,65,66,67,68]. Some researchers have reported that dynamic changes in DNA methylation are involved in the regulation of photoperiod- and/or thermosensitive GMS in rice [69,70,71] and cotton [35,40]; GMS in wheat [38], cabbage [41], and tomato [42]; and CMS in rice [37] and maize [39]. However, the genome-wide cytosine methylation profile and the possible role of DNA methylation in cotton CMS have not been reported so far.…”

“…Conversely, for mitochondria that are actively making ATP and consequently have a lower ∆ p and NADH/NAD + ratio, the extent of O 2 •− production is far lower [84]. Recent research has shown that the expression of genes involved in redox homeostasis and energy metabolism is significantly modulated by DNA methylation in cotton anthers under high-temperature (HT) stress [35,40]. Our KEGG analysis results also found that hyper-DEGs in ZB versus ZBA were significantly enriched in the “oxidative phosphorylation” pathway (Figure 5a and Supplementary Materials, Table S3).…”

“…Emerging evidence has shown that dynamic changes in DNA methylation may mediate transcriptional variation during male reproductive development [35,36]. Over the past several years, the association of DNA methylation status with CMS or genic male sterility (GMS) has been reported in many plants, such as rice [37], wheat [38], maize [39], cotton [35,40], cabbage [41], and tomato [42]. These observations suggest that disrupted genomic DNA methylation in response to high-temperature stress disturbs sugar and ROS metabolism, ultimately resulting in microspore abortion in GMS cotton [35].…”