Lack of the COMPASS Component Ccl1 Reduces H3K4 Trimethylation Levels and Affects Transcription of Secondary Metabolite Genes in Two Plant-Pathogenic Fusarium Species.

Lena Studt,Michael Sulyok,Slavica Janevska,Stefan Boedi,Bettina Tudzynski,Hans-Ulrich Humpf,Joseph Strauss,Birgit Arndt

doi:10.3389/fmicb.2016.02144

Abstract

In the two fungal pathogens Fusarium fujikuroi and Fusarium graminearum, secondary metabolites (SMs) are fitness and virulence factors and there is compelling evidence that the coordination of SM gene expression is under epigenetic control. Here, we characterized Ccl1, a subunit of the COMPASS complex responsible for methylating lysine 4 of histone H3 (H3K4me). We show that Ccl1 is not essential for viability but a regulator of genome-wide trimethylation of H3K4 (H3K4me3). Although, recent work in Fusarium and Aspergillus spp. detected only sporadic H3K4 methylation at the majority of the SM gene clusters, we show here that SM profiles in CCL1 deletion mutants are strongly deviating from the wild type. Cross-complementation experiments indicate high functional conservation of Ccl1 as phenotypes of the respective △ccl1 were rescued in both fungi. Strikingly, biosynthesis of the species-specific virulence factors gibberellic acid and deoxynivalenol produced by F. fujikuroi and F. graminearum, respectively, was reduced in axenic cultures but virulence was not attenuated in these mutants, a phenotype which goes in line with restored virulence factor production levels in planta. This suggests that yet unknown plant-derived signals are able to compensate for Ccl1 function during pathogenesis.

Highlights

Filamentous fungi produce a huge arsenal of secondary metabolites (SMs), small molecular-weight compounds that are not needed for the survival of the fungus but are thought to contribute to the fitness of its producer in some way (Fox and Howlett, 2008; Reverberi et al, 2010; Rohlfs and Churchill, 2011)
Complementation was done by homologous re-integration of the native genes driven by the native promoters into the ffccl1- and fgccl1-mutant backgrounds resulting in three independent mutants each for F. fujikuroi (FfCcl1Cil_T2, T7, T14) and F. graminearum (FgCcl1Cil_T6, T7, T8), that showed identical phenotypes and correct in loco integration of FfCCL1 and FgCCL1, respectively (Supplementary Figure S3A)
Methylation of H3K4 is mediated by the methyltransferase Set1 that catalyzes mono, di- and trimethylation and is itself integrated in the COMPASS complex (Roguev et al, 2001; Krogan et al, 2002; Schneider et al, 2005)

Summary

Introduction

Filamentous fungi produce a huge arsenal of secondary metabolites (SMs), small molecular-weight compounds that are not needed for the survival of the fungus but are thought to contribute to the fitness of its producer in some way (Fox and Howlett, 2008; Reverberi et al, 2010; Rohlfs and Churchill, 2011). The chromatin landscape is either loosely packed, open for transcription (euchromatin) or densely packed and silenced (heterochromatin). Both chromatin states are associated with the activity of certain histone-modifying enzymes that are often part of large enzyme complexes and involved in the addition or removal of residues at defined amino acids of the histone protein tails (e.g., Bannister and Kouzarides, 2011; Gacek and Strauss, 2012)

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Results

Conclusion