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Genome-wide DNA methylation comparison reveals epigenetically regulated regeneration capacity of Boea hygrometrica during development

ABSTRACT: Plants are competent to regenerate new individuals from differentiated tissues under appropriate culture conditions. Although the molecular basis of shoot regeneration has steadily been unraveled, role of DNA methylation in the regulation of plant regeneration capacity remains practically unknown. Here, we established an effective auxin/cytokinin-induced regeneration system of the Chinese resurrection plant Boea hygrometrica through direct organogenesis, and observed that the potential regeneration capacity of leaf explants was gradually decreased with increased age of donor plants. Global transcriptome analysis revealed significant up-regulation of genes required for phenylpropanoid biosynthesis and phytohormone signaling while inhibition of photosynthetic activity in leaf explants during regeneration. Transcriptional changes of positive regulators HY5, STM, EMK and FLA, and negative regulators TSD and CDK involved in plant regeneration, were positively correlated with the regeneration process of B. hygrometrica, implicating their conserved functions across plant species. Comparison of global DNA methylation profiles between expanding young leaves and fully expanded mature leaves with different regeneration capability using whole-genome bisulfite sequencing revealed that increased asymmetrical methylation in mature leaves were predominant distributed in promoter regions, demonstrating their putative inhibitory function for downstream gene expression in B. hygrometrica leaves during maturation. Moreover, the predicted possible DNA methylation control for genes encoding GRCWP1 and BGS40L essential for cell wall architecture, CENL1 controlling extend shoot meristem phases, ANL2 and WRKY75 mediating root hair development, as well as HY5 and two members of ABA signaling components ABF and PP2C also provide new insights into the association of DNA methylation dynamics with regeneration capacity.

ORGANISM(S): Dorcoceras hygrometricum

PROVIDER: GSE119683 | GEO | 2019/11/25

REPOSITORIES: GEO

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Project description:Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimationinduced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B. hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, which may contribute directly or indirectly to the improvement of dehydration tolerance in B. hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation.