Histone Methylation Is Required for Virulence, Conidiation, and Multi-Stress Resistance of Alternaria alternata

Abstract

Histone methylation, which is critical for transcriptional regulation and various biological processes in eukaryotes, is a reversible dynamic process regulated by histone methyltransferases (HMTs) and histone demethylases (HDMs). This study determined the function of 5 HMTs (AaDot1, AaHMT1, AaHnrnp, AaSet1, and AaSet2) and 1 HDMs (AaGhd2) in the phytopathogenic fungus Alternaria alternata by analyzing targeted gene deletion mutants. The vegetative growth, conidiation, and pathogenicity of ∆AaSet1 and ∆AaSet2 were severely inhibited indicating that AaSet1 and AaSet2 play critical roles in cell development in A. alternata. Multiple stresses analysis revealed that both AaSet1 and AaSet2 were involved in the adaptation to cell wall interference agents and osmotic stress. Meanwhile, ∆AaSet1 and ∆AaSet2 displayed serious vegetative growth defects in sole carbon source medium, indicating that AaSet1 and AaSet2 play an important role in carbon source utilization. In addition, ∆AaSet2 colony displayed white in color, while the wild-type colony was dark brown, indicating AaSet2 is an essential gene for melanin biosynthesis in A. alternata. AaSet2 was required for the resistance to oxidative stress. On the other hand, all of ∆AaDot1, ∆AaHMT1, and ∆AaGhd2 mutants displayed wild-type phenotype in vegetative growth, multi-stress resistance, pathogenicity, carbon source utilization, and melanin biosynthesis. To explore the regulatory mechanism of AaSet1 and AaSet2, RNA-seq of these mutants and wild-type strain was performed. Phenotypes mentioned above correlated well with the differentially expressed genes in ∆AaSet1 and ∆AaSet2 according to the KEGG and GO enrichment results. Overall, our study provides genetic evidence that defines the central role of HMTs and HDMs in the pathological and biological functions of A. alternata.

Positive selection and functional diversification of transcription factor Cmr1 homologs in Alternaria

“…Indeed, one IG pathway gene, AbSte7 in A. brassicicola and one CWI pathway gene, AaSLT2 in A. alternata are required for melanin biosynthesis (Yago et al 2021 ; Xu et al 2016 ). In addition, AaSet2 encoding a histone methyltransferase is involved in melanin accumulation (Meng et al 2022 ). Histone methylation is known to be vital for transcriptional regulation and diverse biological processes.…”

The COMPASS Complex Regulates Fungal Development and Virulence through Histone Crosstalk in the Fungal Pathogen Cryptococcus neoformans

“…In higher eukaryotes, misregulation of H3K4 methylation has been implicated in the pathogenesis of cancer and in development defects [ 7 ]. In lower eukaryotes, H3K4 methylation has been shown to be required for morphogenesis, stress responses, secondary metabolism, and pathogenesis, particularly in pathogenic fungi [ 16 , 17 , 19 , 21 , 24 , 25 , 59 ]. The function of the COMPASS complex in mediating H3K4 methylation is highly conserved from yeast to humans; however, variations exist among the subunits of this complex.…”

“…In the plant fungal pathogen Magnaporthe oryzae , MoBre2, MoSpp1, and MoSwd2 function as a complex to methylate H3K4 in the region of the transcriptional start site of target genes that are involved in mycelial growth and the formation of conidia and infectious hyphae [ 16 ]. In Alternaria alternata , one of the most serious phytopathogenic fungi, AaSet1 also plays critical roles in cell development and is involved in the adaptation to cell wall interference agents and osmotic stress [ 17 ]. In Fusarium graminearum , FgSet1 is not only predominantly responsible for H3K4me, but it also plays an important role in response to cell wall-damaging agents via negatively regulating phosphorylation of FgMgv1, a core kinase in the cell wall integrity pathway [ 18 ].…”