H3K4 trimethylation by CclA regulates pathogenicity and the production of three families of terpenoid secondary metabolites in Colletotrichum higginsianum

Abstract

Summary The role of histone 3 lysine 4 (H3K4) methylation is poorly understood in plant pathogenic fungi. Here, we analysed the function of CclA, a subunit of the COMPASS complex mediating H3K4 methylation, in the brassica anthracnose pathogen Colletotrichum higginsianum. We show that CclA is required for full genome‐wide H3K4 trimethylation. The deletion of cclA strongly reduced mycelial growth, asexual sporulation and spore germination but did not impair the morphogenesis of specialized infection structures (appressoria and biotrophic hyphae). Virulence of the ΔcclA mutant on plants was strongly attenuated, associated with a marked reduction in appressorial penetration ability on both plants and inert cellophane membranes. The secondary metabolite profile of the ΔcclA mutant was greatly enriched compared to that of the wild type, with three different families of terpenoid compounds being overproduced by the mutant, namely the colletochlorins, higginsianins and sclerosporide. These included five novel molecules that were produced exclusively by the ΔcclA mutant: colletorin D, colletorin D acid, higginsianin C, 13‐epi‐higginsianin C and sclerosporide. Taken together, our findings indicate that H3K4 trimethylation plays a critical role in regulating fungal growth, development, pathogenicity and secondary metabolism in C. higginsianum.

Metabolomics as an Emerging Tool for the Study of Plant–Pathogen Interactions

“…Interestingly, a genomic and transcriptomics study revealed that different effectors are secreted in each biotrophic or necrotrophic lifestyle [131]. Moreover, more recent integrated research with metabolomics showed that terpenoid production is related to C. higginsianum pathogenesis, the causal agent of antrachnose in a wide spectrum of crops [132,133].…”

The Methyltransferase AflSet1 Is Involved in Fungal Morphogenesis, AFB1 Biosynthesis, and Virulence of Aspergillus flavus

“…As a set domain containing methyltransferase, Set1 is closely binding with 60 (Bre2), Cps50 (Swd1), Cps30 (Swd3) and Cps40 in Y-shaped COMPASS (complex of proteins associated with Set1) (Qu et al, 2018). The homolog of Bre2 in Saccharomyces cerevisiae, CclA was found to play a critical role in H3K4 trimethylation catalyzed by COMPASS complex in Colletotrichum higginsianum (Dallery et al, 2019). The absence of CclA significantly reduces hyphae growth, conidiation and conidium germination, and attenuates the virulence of the fungus on its plant host, but greatly enriches the profile of its secondary metabolites (Dallery et al, 2019).…”

“…The homolog of Bre2 in Saccharomyces cerevisiae, CclA was found to play a critical role in H3K4 trimethylation catalyzed by COMPASS complex in Colletotrichum higginsianum (Dallery et al, 2019). The absence of CclA significantly reduces hyphae growth, conidiation and conidium germination, and attenuates the virulence of the fungus on its plant host, but greatly enriches the profile of its secondary metabolites (Dallery et al, 2019). FgSet1 is involved in the methylation of H3K4 in Fusarium graminearum, and plays an important role in mycelium growth, mycotoxin biosynthesis, and virulence in the fungus (Liu et al, 2015).…”

Transcriptome Analysis Identifies a Gene Cluster for the Biosynthesis of Biruloquinone, a Rare Phenanthraquinone, in a Lichen-Forming Fungus Cladonia macilenta

“…These chemotypic variations may be attributable to phe-notypic instability of isolated mycobionts. A significant proportion of biosynthetic gene clusters in fungi remain silenced in normal growth conditions and are subject to tight controls by epigenetic regulators (e.g., histone modifiers) [54][55][56][57][58][59][60][61][62][63]. Thus, it is conceivable that the biruloquinone BGC was derepressed by dysfunctionally regulated histone modifiers due to genomic instability of isolated mycobionts, which otherwise remains silenced during the symbiosis.…”