|ELMORE, M. HOLLY - Vanderbilt University|
|MCGARY, KRISTON - Vanderbilt University|
|WISECAVER, JENNIFER - Vanderbilt University|
|SLOT, JASON - Vanderbilt University|
|GEISER, DAVID - Pennsylvania State University|
|O Donnell, Kerry|
|ROKAS, ANTONIS - Vanderbilt University|
Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/2/2015
Publication Date: 2/6/2015
Publication URL: http://handle.nal.usda.gov/10113/60627
Citation: Elmore, M., McGary, K.L., Wisecaver, J.H., Slot, J.C., Geiser, D.M., Sink, S.L., O'Donnell, K., Rokas, A. 2015. Clustering of two genes involved in cyanate detoxification evolved recently and independently in multiple fungal lineages. Genome Biology and Evolution. 7(3):789-800.
Interpretive Summary: Using a comparative genomics approach, we discovered that a two-gene cluster potentially conferring resistance to cyanate-based fungicides, the most effective fumigants currently available, arose independently in three distantly related fungal lineages. We identified a novel putative cyanate resistance gene cluster (CR cluster) in these fungi comprised of duplicated genes, traced its evolution within a cosmopolitan group of agronomically important vascular wilt plant pathogens (i.e., the Fusarium oxysporum species complex (FOSC)). Genome-wide surveys within the FOSC indicated that the CR cluster varied in copy number across isolates. Interestingly, CR cluster copies within this complex were always found on small chromosomes that tended to be enriched in genes associated with plant pathogenicity. Evolutionary diversification of the CR cluster in 163 FOSC strains from a wide variety of hosts suggested a recent history of rampant transfers between isolates. Independent evolution of the CR gene cluster in three distantly related fungal lineages and its spread across the FOSC both suggest that this cluster evolved in response to a selection pressure that is likely global and recent. We speculate that this selection pressure is the recent introduction of cyanate fungicides in global agricultural. This finding is important because cyanate fungicides comprise the most popular and effective fumigants available for controlling soil-borne plant pathogens. This research will be of interest to a wide range of agricultural scientists interested in controlling plant pathogenic fungi with fungicides.
Technical Abstract: Fungi that have the enzymes cyanase and carbonic anhydrase show a limited capacity to detoxify cyanate, a fungicide employed by both plants and humans. Here, we describe a novel two-gene cluster that comprises duplicated cyanase and carbonic anhydrase copies, which we name the CCA gene cluster, trace its evolution across Ascomycetes, and examine the evolutionary dynamics of its spread among lineages of the Fusarium oxysporum species complex (hereafter referred to as the FOSC), a cosmopolitan clade of purportedly clonal vascular wilt plant pathogens. Phylogenetic analysis of fungal cyanase and carbonic anhydrase genes reveals that the CCA gene cluster arose independently at least twice and is now present in three lineages, namely Cochliobolus lunatus, Oidiodendron maius, and the FOSC. Genome-wide surveys within the FOSC indicate that the CCA gene cluster varies in copy number across isolates, is always located on accessory chromosomes, and is absent in FOSC’s closest relatives. Phylogenetic reconstruction of the CCA gene cluster in 163 FOSC strains from a wide variety of hosts suggests a recent history of rampant transfers between isolates. We hypothesize that the independent formation of the CCA gene cluster in different fungal lineages and its spread across FOSC strains may be associated with resistance to plant-produced cyanates or to use of cyanate fungicides in agriculture.