Abstract
SummaryThe 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.
Highlights
Fungi are rich sources of bioactive natural products with high value for the pharmaceutical industry (Andersen et al, 2013; Wiemann and Keller, 2014)
Our findings demonstrate that chromatin remodelling mediated by CclA contributes to regulating secondary metabolism and pathogenicity in C. higginsianum
H3K4 trimethylation was restored to wild-type levels in the complemented strain C10 (Fig. 1A). These results show that CclA is required for full H3K4 trimethylation in C. higginsianum, as was found previously with CclA/Bre2 mutants in A. thaliana (Jiang et al, 2011), Schizosaccharomyces pombe (Mikheyeva et al, 2014), Aspergillus oryzae (Shinohara et al, 2016) and Fusarium spp. (Studt et al, 2017)
Summary
Fungi are rich sources of bioactive natural products (mostly secondary metabolites) with high value for the pharmaceutical industry (e.g. paclitaxel, penicillin, cyclosporins and statins) (Andersen et al, 2013; Wiemann and Keller, 2014). Alteration of the chromatin landscape by genetic manipulation of histone-modifying enzymes has proven to be a productive approach to identify new secondary metabolism (SM) products in numerous fungi (Chiang et al, 2009; Brakhage, 2013; Wu and Yu, 2015). In Epichloe festucae, the loss of trimethylation of histone protein H3 at lysine 9 (H3K9me3) or lysine 27 (H3K27me3) in the promoter regions of SM genes activated their expression in vitro and was needed for the mutualistic interaction of this endophyte with Lolium perenne (Chujo and Scott, 2014).
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