Comparative Transcriptome Analysis Revealed Genes Regulated by Histone Acetylation and Genes Related to Sex Hormone Biosynthesis in Phytophthora infestans

Abstract

Late blight caused by Phytophthora infestans, is one of the most devastating diseases of potato, and was responsible for the death of millions of people during the Irish Potato Famine in the nineteenth century. Phytophthora infestans is a heterothallic oomycete that typically requires two compatible types (mating types), A1 and A2, to complete sexual reproduction (i.e., oospore production). Oospores have critical effects on disease epidemiology because they serve as the primary inoculum in subsequent growing seasons. The sexual reproduction of Phytophthora species is regulated by α hormones. In previous studies, we proved that transformants in which selected histone deacetylase (HDAC) genes are silenced exhibit abnormal hormone production. In the current study, we compared the transcriptomes of HDAC-silenced and wild-type strains to explore the genes regulated by HDAC and the genes involved in sex hormone biosynthesis in Phytophthora species. A total of 14,423 transcripts of unigenes were identified in the wild-type strain, the HDAC family-silenced transformant (HDST), and the HDAC7-silenced transformant (H7ST). After comparing the intergroup gene expression levels, 1,612 unigenes were identified as differentially expressed among these strains. The expression levels of 16 differentially expressed genes (DEGs) were validated by quantitative realtime PCR. The functional annotation of the DEGs by gene ontology and Kyoto Encyclopedia of Genes and Genomes pathway analyses indicated that HDACs affect the expression of genes related to metabolic and biosynthetic processes, RNA processing, translation, ribosome biogenesis, cellular structural constituents, RNA binding, and protein binding. Moreover, HDAC7 specifically influences the transcription of genes associated with transport, methylation, mitochondria, organelle inner membranes, receptors and transporters, and hydrolase activities. We also identified 18 candidate genes related to α hormones biosynthesis, including a gene encoding the NF-Y transcription factor (PITG_10861). The overexpression of

Epigenetic insight into regulatory role of chromatin covalent modifications in lifecycle and virulence of Phytophthora

“…1). Most of the experimental evidence focuses on the analysis of enzymes involved in CCMs such as HATs, HDCAs and KMTs, as well as their expression levels at different stages of Phytophthora lifecycle (Wang et al ., 2016; Tzelepis et al ., 2020; Wang et al ., 2020a; Wang et al ., 2020c). The enzymes involved in CCMs seem to be encoded in the genomes of the most destructive Phytophthora species (Wang et al ., 2016) and their expression levels change in response to environmental stress, development stages, sexual and asexual reproduction, and host adaptation.…”

“…Recently, the transcriptomic analysis of an HDAC‐silenced P . infestans strain revealed several biological processes regulated by histone deacetylation (Wang et al ., 2020c), including the biosynthesis of the diterpenic sex hormones α1 and α2, essential molecules for sexual reproduction and secreted by mating types A1 and A2 respectively (Ojika et al ., 2011). Expression in HDAC‐silenced transformants was affected in the genes involved in the terpenoid backbone biosynthesis mediated by the mevalonate pathway, transcription factors and enzymes that modify chemical groups in the structure of hormones.…”

Histone (de)acetylation in epigenetic regulation of Phytophthora pathobiology

“…Type A is involved in processes related to transcription by modification of specific lysine residues on histone tails, whereas type B is responsible for the acetylation of newly synthesized histones before their assembly into nucleosomes (Camilo & Jerónimo, 2020 ). Moreover, type A HATs are further divided into five prominent families: GNAT (GCN‐related N‐acetyltransferase), MYST (MOZ, Ybf2/Sas3, Sas2, and Tip60), p300/CREB‐binding protein (CBP), transcription initiation factor TAFII‐250, and nuclear receptor cofactors (Jeon et al., 2014 ; Wang, Lv, et al., 2020 ). HATs belonging to these families have been well‐studied in filamentous fungi.…”

Genome-wide analyses of histone modifications and chromatin accessibility reveal the distinct genomic compartments in the Irish potato famine pathogen Phytophthora infestans

“…Recently, ChIP-seq based on the H3 variant CenH3 (CENP-A) uncovered the centromeres in P. sojae, which lack H3K4me2 but embed within the heterochromatin marks H3K9me3 and H3K27me3 [29]. In silico, several histone modification enzymes were identified in Phytophthora, including histone acetyltransferases (HATs), deacetylases (HDACs) [30], some of which were involved in metabolic and biosynthetic process, sexual reproduction and virulence [31,32]. In addition, gene silencing has been shown to be mediated by multiple different mechanisms, and be an effective way for oomycete pathogens to modulate virulence factors [33][34][35].…”