Cyst Nematode Parasitism Induces Dynamic Changes in the Root Epigenome

Abstract

A growing body of evidence indicates that epigenetic modifications can provide efficient, dynamic, and reversible cellular responses to a wide range of environmental stimuli. However, the significance of epigenetic modifications in plant-pathogen interactions remains largely unexplored. In this study, we provide a comprehensive analysis of epigenome changes during the compatible interaction between the beet cyst nematode Heterodera schachtii and Arabidopsis (Arabidopsis thaliana). Whole-genome bisulfite sequencing was conducted to assess the dynamic changes in the methylome of Arabidopsis roots in response to H. schachtii infection. H. schachtii induced widespread hypomethylation of protein-coding genes and transposable elements (TEs), preferentially those adjacent to protein-coding genes. The abundance of 24-nt siRNAs was associated with hypermethylation of TEs and gene promoters, with influence observed for methylation context and infection time points. mRNA sequencing revealed a significant enrichment for the differentially methylated genes among the differentially expressed genes, specifically those with functions corresponding to primary metabolic processes and responses to stimuli. The differentially methylated genes overlapped with more than one-fourth of the syncytium differentially expressed genes and are of functional significance. Together, our results provide intriguing insights into the potential regulatory role of differential DNA methylation in shaping the biological interplay between cyst nematodes and host plants.

Silenced retrotransposons are major rasiRNAs targets in Arabidopsis galls induced by Meloidogyne javanica

“…The functional role of the differentially accumulated rasiRNAs in galls and syncytia (Hewezi et al., ; this article) in TE regions, which are also differentially regulated in infected tissues vs. their corresponding uninfected control tissues, is still an interesting open field of study. In line with our data, the abundance of 24‐nucleotide rasiRNAs was associated with the hypermethylation of TEs and gene promoters during the interaction of Arabidopsis with cyst nematodes (Hewezi et al., ; Piya et al., ). Further experiments are required to correlate our results in galls with methylation at these sites and to understand their implications to gall development at the early stages of infection.…”

“…sRNA libraries from Arabidopsis galls induced by M. javanica ; 3 dpi) and M. incognita (Medina et al, 2017; 7 and 14 dpi), as well as syncytia induced by the cyst nematode H. schachtii (Hewezi et al, 2008;4 and 7 dpi;Hewezi et al, 2017; 5 and 10 dpi), presented a significant enrichment in 24nucleotide sRNAs compared with control root libraries. In previous work by Cabrera et al (2016b), an analysis of sRNA length distribution suggested that the abundance of 24-nucleotide sRNAs constituted a gall hallmark, at least at early infection stages, whereas 21-nucleotide sRNAs (the length of most plant miRNAs; Axtell, 2013;Xie et al, 2015) were more abundant in uninfected roots.…”

“…sRNA libraries from Arabidopsis galls induced by M. javanica (Cabrera et al., ; 3 dpi) and M. incognita (Medina et al., ; 7 and 14 dpi), as well as syncytia induced by the cyst nematode H. schachtii (Hewezi et al., ; 4 and 7 dpi; Hewezi et al., ; 5 and 10 dpi), presented a significant enrichment in 24‐nucleotide sRNAs compared with control root libraries. In previous work by Cabrera et al.…”

“…Recently, Hewezi et al. () have reported that 24‐nucleotide rasiRNAs are highly abundant in the syncytia formed by the cyst nematode Heterodera schachtii and are accumulated in hypermethylated regions of the genome (Hewezi et al., ). A similar analysis of Meloidogyne javanica galls is still lacking.…”

The role of plant epigenetics in biotic interactions

“…A. thaliana roots infected by the cyst nematode Heterodera schachtii showed large-scale changes in DNA methylation and small RNA populations, with dynamic shifts across the infection stages. Although DNA methylation changes were probably over-estimated due to lenient calling of differentially methylated regions, epigenetic changes appeared to be associated with transcriptional changes of defense-related genes in the root (Hewezi et al, 2017).…”