H3K27me3 is vital for fungal development and secondary metabolite gene silencing, and substitutes for the loss of H3K9me3 in the plant pathogen Fusarium proliferatum

Facultative heterochromatin marked by histone H3 lysine 27 trimethylation (H3K27me3) is an important regulatory layer for secondary metabolite (SM) gene silencing and important for fungal development in the genus Fusarium. While this histone mark is essential in some (e.g., the rice pathogen Fusarium fujikuroi), it appears dispensable in other fusaria. Here, we show that deletion of FpKMT6 is detrimental but not lethal in the plant pathogen Fusarium proliferatum, a member of the Fusarium fujikuroi species complex (FFSC). Loss of FpKmt6 results in aberrant growth, and expression of a large set of previously H3K27me3-silenced genes is accompanied by increased H3K27 acetylation (H3K27ac) and an altered H3K36me3 pattern. Next, H3K9me3 patterns are affected in delta-fpkmt6, indicating a crosstalk between both heterochromatic marks that became even more obvious in a strain deleted for FpKMT1 encoding the H3K9-specific histone methyltransferase. In delta-fpkmt1, all H3K9me3 marks present in the wild-type strain are replaced by H3K27me3, a finding that possibly explains the subtle phenotype of delta-fpkmt1 strains which stands in marked contrast to other filamentous fungi. A large proportion of SM-encoding genes is allocated with H3K27me3 in the wild-type strain, and loss of H3K27me3 result in elevated expression of 49% of them. Interestingly, genes involved in the biosynthesis of the phytohormones gibberellins (GA) are among the most upregulated genes in delta-fpkmt6. Although several FFSC members harbor GA biosynthetic genes, its production in planta is largely restricted to F. fujikuroi with few exceptions. We show that GA gene silencing is mediated by H3K27me3 in F. proliferatum and in at least one additional FFSC member, possibly outlining the distinct lifestyles of these notorious plant pathogens.

以组蛋白H3赖氨酸27三甲基化（H3K27me3）标记的兼性异染色质（facultative heterochromatin）是调控镰孢菌属（Fusarium）次级代谢产物（SM）基因沉默的关键表观遗传层级，同时对该属真菌的发育至关重要。该组蛋白修饰在部分镰孢菌（如水稻致病菌藤仓镰孢菌（Fusarium fujikuroi））中不可或缺，但在其他镰孢菌中似乎并非必需。本研究表明，在植物致病菌增殖镰孢菌（Fusarium proliferatum，藤仓镰孢菌物种复合体（FFSC）的成员之一）中，敲除FpKMT6会产生有害但非致死的表型。FpKmt6的缺失会导致菌株生长异常，大量先前被H3K27me3沉默的基因表达上调，同时伴随H3K27乙酰化（H3K27ac）水平升高以及H3K36me3修饰模式改变。FpKMT6基因缺失突变株中H3K9me3的修饰模式也受到影响，表明两类异染色质修饰标记之间存在串扰；这种串扰在同时敲除编码H3K9特异性组蛋白甲基转移酶（histone methyltransferase）的FpKMT1的菌株中更为显著。在FpKMT1基因缺失突变株中，野生型菌株中所有的H3K9me3标记均被H3K27me3取代，这一发现或可解释该突变株表型微弱的原因，这与其他丝状真菌的表型形成鲜明对比。野生型菌株中，大量编码次级代谢产物的基因带有H3K27me3标记，而H3K27me3的缺失会导致其中49%的基因表达上调。有趣的是，参与植物激素赤霉素（GA）生物合成的基因是FpKMT6基因缺失突变株中上调幅度最高的基因之一。尽管多个FFSC成员均携带赤霉素生物合成基因，但在植物体内的赤霉素产生几乎仅局限于藤仓镰孢菌，仅有少数例外。本研究证实，在增殖镰孢菌以及至少另一种FFSC成员中，赤霉素基因的沉默由H3K27me3介导，这或许可以阐明这些臭名昭著的植物病原菌的不同生活方式。