Genome-Wide Annotation and Comparative Analysis of Cytochrome P450 Monooxygenases in Basidiomycete Biotrophic Plant Pathogens

Abstract

Fungi are an exceptional source of diverse and novel cytochrome P450 monooxygenases (P450s), heme-thiolate proteins, with catalytic versatility. Agaricomycotina saprophytes have yielded most of the available information on basidiomycete P450s. This resulted in observing similar P450 family types in basidiomycetes with few differences in P450 families among Agaricomycotina saprophytes. The present study demonstrated the presence of unique P450 family patterns in basidiomycete biotrophic plant pathogens that could possibly have originated from the adaptation of these species to different ecological niches (host influence). Systematic analysis of P450s in basidiomycete biotrophic plant pathogens belonging to three different orders, Agaricomycotina (Armillaria mellea), Pucciniomycotina (Melampsora laricis-populina, M. lini, Mixia osmundae and Puccinia graminis) and Ustilaginomycotina (Ustilago maydis, Sporisorium reilianum and Tilletiaria anomala), revealed the presence of numerous putative P450s ranging from 267 (A. mellea) to 14 (M. osmundae). Analysis of P450 families revealed the presence of 41 new P450 families and 27 new P450 subfamilies in these biotrophic plant pathogens. Order-level comparison of P450 families between biotrophic plant pathogens revealed the presence of unique P450 family patterns in these organisms, possibly reflecting the characteristics of their order. Further comparison of P450 families with basidiomycete non-pathogens confirmed that biotrophic plant pathogens harbour the unique P450 families in their genomes. The CYP63, CYP5037, CYP5136, CYP5137 and CYP5341 P450 families were expanded in A. mellea when compared to other Agaricomycotina saprophytes and the CYP5221 and CYP5233 P450 families in P. graminis and M. laricis-populina. The present study revealed that expansion of these P450 families is due to paralogous evolution of member P450s. The presence of unique P450 families in these organisms serves as evidence of how a host/ecological niche can influence shaping the P450 content of an organism. The present study initiates our understanding of P450 family patterns in basidiomycete biotrophic plant pathogens.

Heterologous coexpression of the benzoate‐para‐hydroxylase CYP53B1 with different cytochrome P450 reductases in various yeasts

“…Further demonstration of the complicated nature of P450-CPR interactions was obtained in a fascinating study by Lah et al (2011). Many fungal species contain only one CPR regardless of the number of P450s present (Lah et al, 2008), including ascomycetous Pezizomycotina and basidiomycetous Agaricomycotina, which can encode hundreds of potential P450s in their genomes (Lah et al, 2008(Lah et al, , 2011Qhanya et al, 2015). One CPR is therefore capable of supporting numerous P450s, although in certain organisms more CPRs are present.…”

“…The hydroxylation of benzoic acid (BA) and its derivatives is a critical step in degradation of structural and protective compounds of plants, and as such these enzymes have been linked to persistence and pathogenesis of fungi to plants (Jawallapersand et al, 2014;Durairaj et al, 2016). In fact, this is one of three P450 families highly conserved among biotrophic plant pathogenic fungi, with the other two families involved in membrane ergosterol biosynthesis, highlighting their importance (Qhanya et al, 2015). As such, they have been identified as potential targets for antifungal drugs (Jawallapersand et al, 2014;Koro sec et al, 2014).…”

Puccinia triticina pathotypes-THTT and THTS display complex transcript profiles on Thatcher

“…CYP53 family members play a key role in fungal colonization of plant material by detoxification of anti-fungal compounds released by plants or generated during plant material degradation. Moreover, CYP53 family members play a role in the generation of a secondary metabolite, veratryl alcohol, which is crucial in the degradation of the plant cell wall component, lignin [29]. The expression of Unigene18727_Tc15_2 peaked in THTT at 12 hpi and gradually increases and peaks at 72 hpi in THTS, Further, it hardly expresses at later stage.…”

Fungal Genomes and Insights into the Evolution of the Kingdom

“…The p450 monoxygenase family is also highly expanded in mushroom-forming fungi, especially in white rot fungi such as Phanerochaete , which likely allow it to degrade a rich collection of substrates including lignin [63,152,156]. These expansions may have been important in niche adaptations and the evolution of specific traits such as lignin modifications and degradation, decomposition of complex hydrocarbons, and the ability to growth as a biotrophic plant pathogen [157–163]. …”