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

Author
item KARAGIANNI, ELENI - Democritus University Of Thrace
item KONTOMINA, EVANTHIA - Democritus University Of Thrace
item DAVIS, BRITTON - University Of Georgia
item KOTSELI, BARBARA - Democritus University Of Thrace
item TSIRKA, THEODORA - Democritus University Of Thrace
item GAREFALAKI, VASILIKI - Democritus University Of Thrace
item SIM, EDITH - University Of Oxford
item Glenn, Anthony - Tony
item BOUKOUVALA, SOTIRIA - Democritus University Of Thrace

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/6/2015
Publication Date: 8/6/2015
Citation: Karagianni, E.P., Kontomina, E., Davis, B., Kotseli, B., Tsirka, T., Garefalaki, V., Sim, E., Glenn, A.E., Boukouvala, S. 2015. Homologues of xenobiotic metabolizing N-acetyltransferases in plant-associated fungi: Novel functions for an old enzyme family. Scientific Reports. 5:12900.

Interpretive Summary: Fungi that are pathogenic on plants produce and release a diverse mixture of metabolites that can negatively impact the health of the plant. Similarly, plants also produce metabolites that serve as chemical deterrents to inhibit the growth or even kill pathogenic fungi and bacteria that may attempt to infect the plants. In each case, the fungus or the plant often defends itself by metabolizing or detoxifying the chemical compounds. The compounds are generally referred to as xenobiotics. We have investigated one particular class of xenobiotic metabolizing enzyme, arylamine N-acetyltransferase (NAT), in five different fungi. These fungi were three species of Fusarium and two species of Aspergillus. Two of the Fusarium species and one of the Aspergillus species produce mycotoxins that are a food safety concern since these all three species are capable of infecting corn and other grain and nut commodities. We document the functional diversification of NAT enzymes in these fungi and identify three functional groups. The first NAT enzyme group is found in all species and catalyzes reactions with acetyl-CoA or propionyl-CoA. The second group is restricted to the plant pathogens and is active with malonyl-CoA, particularly in Fusarium species infecting cereals. The third group generates minimal activity and has uncertain function. We propose that fungal NAT enzymes may have evolved to perform diverse functions, potentially relevant to pathogen fitness, acetyl-CoA/propionyl-CoA intracellular balance, and the production of secondary metabolites such as mycotoxins, pigments, and other compounds.

Technical 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 defense 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.