Integrated transcriptome and methylome analyses reveal the molecular regulation of drought stress in wild strawberry (Fragaria nilgerrensis)

Abstract

Background Fragaria nilgerrensis, which is a diploid wild strawberry with excellent drought-resistance, would provide useful candidate genes for improving drought resistance of cultivated strawberry. So far, its molecular regulatory networks involved in drought stress are unclear. We therefore investigated the drought response regulatory networks of F. nilgerrensis based on the integrated analysis of DNA methylation, transcriptome and physiological traits during four time points under drought stress. Results The most differentially expressed genes and the physiological changes were found at 8 days (T8) compared with 0 day (T0, control). Methylome analysis revealed slight dynamic changes in genome-wide mC levels under drought conditions, while the most hypomethylated and hypermethylated regions were identified at T4 and T8. Association analysis of the methylome and transcriptome revealed that unexpressed genes exhibited expected hypermethylation levels in mCHG and mCHH contexts, and highly expressed genes exhibited corresponding hypomethylation levels in the gene body, but mCG contexts showed the opposite trend. Then, 835 differentially methylated and expressed genes were identified and grouped into four clustering patterns to characterize their functions. The genes with either negative or positive correlation between methylation and gene expression were mainly associated with kinases, Reactive Oxygen Species (ROS) synthesis, scavenging, and the abscisic acid (ABA) signal pathway. Consistently, weighted gene co-expression network analysis (WGCNA) revealed Hub genes including NCED, CYP707A2, PP2Cs and others that play important roles in the ABA signaling pathway. Conclusion F. nilgerrensis drought is dominated by ABA-dependent pathways, possibly accompanied by ABA-independent crosstalk. DNA methylation may affect gene expression, but their correlation was more subtle and multiple types of association exist. Maintaining the balance between ROS regeneration and scavenging is an important factor in drought resistance in F. nilgerrensis. These results deepen our understanding of drought resistance and its application in breeding in strawberry plants.

DNA methylation regulates the secondary metabolism of saponins to improve the adaptability of Eleutherococcus senticosus during drought stress

“…A growing body of research indicates that modifications to the levels of secondary metabolites accumulated [ 29 – 30 ] and DNA methylation status of the genome and functional genes [ 31 – 32 ] are essential for plant adaptation to drought stress. Uncertainty exists regarding the precise method by which DNA methylation controls plant secondary metabolism during drought.…”

“…Similar characteristics were shown in E. senticosus , wherein at 50% water content, the ideal level for saponin accumulation, some triterpene saponins were greatly increased, and others were significantly decreased. This is mainly because plants first produce secondary metabolic upstream chemicals with very modest molecular weights in response to water scarcity [ 31 ]. More -OH, -OCH 3, and unsaturated double bonds are present in these upstream compounds, which can directly and quickly increase the antioxidant capability of cells [ 41 ].…”

“…More -OH, -OCH 3, and unsaturated double bonds are present in these upstream compounds, which can directly and quickly increase the antioxidant capability of cells [ 41 ]. However, these upstream antioxidant active products become complex compounds like downstream saponins and are retained when drought stress continues [ 31 ]. Simultaneously, varying drought stress levels elicited distinct oxidative stress responses [ 29 ], leading to variations.…”

Recent Advances in The Plant Genomic DNA Methylation Studies and Its Involvement in Regulating Drought Stress Response in Crops

“…In most eukaryotes, the frequent DNA methylation is usually occurs in the cytosine base, which contains CG, CHG and CHH (H for A, T or C) in total three types [18]. Among these three types, the CG methylation level is significantly higher than the CHG or CHH methylation types [23]. CG methylation can occur in the promoter region and part of the pre-transcriptional region, as well as in the 3' end and part of the post-transcriptional region and may inhibit gene expression.…”

DNA methylation participates in drought stress memory and response to drought in Medicago ruthenica

“…In rice, 70% of drought-induced epigenetic methylation sites are demethylated, and stress exposure during the reproductive stage leads to a negative correlation between yield and methylation rate, indicating critical crosstalk between epigenetic and reproductive signals in rice plants under drought stress [50,51]. DNA methylation in wild strawberries (Fragaria nilgerrensis) under drought stress may affect gene expression, regulating osmotic capacity and maintaining a balance between reactive oxygen species regeneration and clearance through ABA-dependent signaling pathways, thereby affecting plant drought tolerance [52]. In this study, we found that M. ruthenica genomic methylation levels decreased after two drought stress exposures, which may have triggered 'priming' stress mechanisms in the plants.…”