Homologues of xenobiotic metabolizing N-acetyltransferases in plant-associated fungi: Novel functions for an old enzyme family

Abstract

Plant-pathogenic fungi and their hosts engage in chemical warfare, attacking each other with toxic products of secondary metabolism and defending themselves via an arsenal of xenobiotic metabolizing enzymes. One such enzyme is homologous to arylamine N-acetyltransferase (NAT) and has been identified in Fusarium infecting cereal plants as responsible for detoxification of host defence compound 2-benzoxazolinone. Here we investigate functional diversification of NAT enzymes in crop-compromising species of Fusarium and Aspergillus, identifying three groups of homologues: Isoenzymes of the first group are found in all species and catalyse reactions with acetyl-CoA or propionyl-CoA. The second group is restricted to the plant pathogens and is active with malonyl-CoA in Fusarium species infecting cereals. The third group generates minimal activity with acyl-CoA compounds that bind non-selectively to the proteins. We propose that fungal NAT isoenzymes may have evolved to perform diverse functions, potentially relevant to pathogen fitness, acetyl-CoA/propionyl-CoA intracellular balance and secondary metabolism.

Biotransformation of 2,4-dinitroanisole by a fungal Penicillium sp.

“…This is in contrast to the findings of Perreault and co-workers, who observed hydroxylamine acetylation with subsequent de-hydroxylation to form 2-NAc-NAN (Perreault et al 2012). The N -acetylation reaction is known to be catalyzed by N -acetyltransferases, which are ubiquitous in fellow plant-derived Ascomycota fungi (Karagianni et al 2015) and detoxify a range of other aromatic amines (Martins et al 2009). An ascomycete fungus detoxified soil artificially contaminated by 3,4-dichloroaniline by N -acetylation to the extent that plants could then grow, indicating that this reaction likely reduces the toxicity of the DNAN metabolite (Martins et al 2009).…”

“…Plant-associated fungi have been shown to perform the N -malonylation reaction on structurally similar aryl amines produced by plants to kill unwanted microorganisms. The fungi have adapted to detoxify these aryl amines, so M254a and b likely result from this known malonyl-transferase-mediated reaction (Karagianni et al 2015). All of the N -acylated metabolites are likely to undergo amide hydrolysis and be back-transformed to primary and secondary amines (Helbling et al 2010), which may explain why most did not accumulate in the media (Fig.…”

Transcriptome‐based analyses of phosphite‐mediated suppression of rust pathogens Puccinia emaculata and Phakopsora pachyrhizi and functional characterization of selected fungal target genes

“…This approach identified two Pe genes that encode glutamate N-acetyltransferase and cystathionine gamma-synthase to have a role in virulence ( Figure 5). N-acetyltransferases are related to pathogen fitness and have detoxifying activities in the host (Karagianni et al, 2015). Cystathionine gammasynthase is particularly interesting because Fusarium graminearum mutants for cystathionine gamma-synthase have reduced virulence, impaired germination of conidia (by 90%), low levels of deoxynivalenol and increased sensitivity to a sterol demethylation inhibitor fungicide, tebuconazole (Fu et al, 2013).…”

Two Horizontally Transferred Xenobiotic Resistance Gene Clusters Associated with Detoxification of Benzoxazolinones by Fusarium Species

“…Further, the FDB2 cluster gene, NAT1 , encodes a member of the arylamine N -acetyltransferase (NAT) family and is essential for transformation of 2-aminophenol (2AP) to HPMA [ 7 ]. Nat1 is unique for the NAT family in that it is a N -malonyltransferase with specificity for malonyl-CoA instead of acetyl-CoA [ 12 ]. We originally designated this gene FDB2 but have recently adopted the designation NAT1 to more clearly associate it with the NAT family and to facilitate clearer annotation of other NAT paralogs in F .…”