Genome-wide analysis of three histone marks and gene expression in Paulownia fortunei with phytoplasma infection

Abstract

BackgroundPaulownia withes’-broom (PaWB) disease caused by phytoplasma is a serious infectious disease for Paulownia. However, the underlying molecular pathogenesis is not fully understood. Recent studies have demonstrated that histone modifications could play a role in plant defense responses to pathogens. But there is still no available genome-wide histone modification data in non-model ligneous species infected with phytoplasma.ResultsHere, we provided the first genome-wide profiles of three histone marks (H3K4me3, H3K36me3 and H3K9ac) in Paulownia fortunei under phytoplasma stress by using chromatin immunoprecipitation sequencing (ChIP-Seq). We found that H3K4me3, H3K36me3 and H3K9ac were mainly enriched in the genic regions in P. fortunei with (PFI) and without (PF) phytoplasma infection. ChIP-Seq analysis revealed 1738, 986, and 2577 genes were differentially modified by H3K4me3, H3K36me3 and H3K9ac marks in PFI under phytoplasma infection, respectively. The functional analysis of these genes suggested that most of them were mainly involved in metabolic pathways, biosynthesis of secondary metabolites, phenylpropanoid biosynthesis, plant-pathogen interaction and plant hormone signal transduction. In addition, the combinational analysis of ChIP-Seq and RNA-Seq showed that differential histone methylation and acetylation only affected a small subset of phytoplasma-responsive genes.ConclusionsTaken together, this is the first report of integrated analysis of histone modifications and gene expression involved in Paulownia-phytoplasma interaction. Our results will provide the valuable resources for the mechanism studies of gene regulation in non-model plants upon pathogens attack.Electronic supplementary materialThe online version of this article (10.1186/s12864-019-5609-1) contains supplementary material, which is available to authorized users.

Genome-wide shifts in histone modifications at early stage of rice infection with Meloidogyne graminicola

“…For example, in bean plants infected with rust pathogen Uromyces appendiculatus, H3K9me2 and H4K12ac showed strong unilateral modification and similar to our data, transcription factors from the WRKY, MYB and bZIP families were affected by these marks (Ayyappan et al, 2015). In another study on Paulownia fortune upon infection by phytoplasma, 1,788 and 939 genomic regions were hyper-and hypoacetylated at H3K9 (Yan et al, 2019). Although a sharp hyperacetylation was not observed the peaks reported in that study were also related with GO terms metabolic process, cellular process and response to stimulus, as seen in our data (Figure 4) (Yan et al, 2019).…”

“…In another study on Paulownia fortune upon infection by phytoplasma, 1,788 and 939 genomic regions were hyper-and hypoacetylated at H3K9 (Yan et al, 2019). Although a sharp hyperacetylation was not observed the peaks reported in that study were also related with GO terms metabolic process, cellular process and response to stimulus, as seen in our data (Figure 4) (Yan et al, 2019). As expected based on the results of the chemical inhibitors and transgenic lines, many defence related genes were marked by the studied histone marks ( Figure 5).…”

“…The involvement of H3K9 acetylation (H3K9ac), a gene activation mark, in plant defence against fungi and bacteria was studied before (Yan et al, 2019). Here, galls at 3 dpi and corresponding root tips were collected and were used for chromatin immunoprecipitation following DNA sequencing.…”

“…Modifications of histone tails are a major mechanism in gene expression regulation, and their role in plant responses to environmental stimuli and pathogen infection has been described (Zhou et al, 2005;Kim et al, 2008;Jaskiewicz et al, 2011;Choi et al, 2012;Li et al, 2013;Dutta et al, 2017;Vijayapalani et al, 2018). For example, upon infection of Paulownia fortunei with phytoplasma, 1788 and 939 genomic regions were hyper-and hypoacetylated, respectively for H3K9ac (Yan et al, 2019). Application of salicylic acid (SA)analogue Benzothiadiazole (BTH) induced H3K9ac enrichment in the promoter of pathogenesis-related gene 1 (PR1) (Lopez et al, 2011).…”

Molecular memory of Flavescence dorée phytoplasma in recovering grapevines

“…Epigenetic marks underlying defence mechanisms in grapevine are still hotly debated 21 and to our knowledge, there are no studies exploring naturally occurring patterns of DNA methylation associated to recovery from phytoplasma infection in field-grown plants. Indeed, available information takes into account either effect of artificially induced DNA methylation in phytoplasma-infected plants maintained under controlled greenhouse conditions 47 or histone modifications occurring in in vitro-cultured phytoplasma-diseased plantlets 48 . Changes in DNA methylation patterns were analysed only on in vitro periwinkle plants exposed to exogenous auxin treatment, in order to investigate effects of hormonal treatments on recovery induction 49 .…”