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

Glenn, Anthony E.; Davis, C. Britton; Gao, Minglu; Gold, Scott E.; Mitchell, Trevor R.; Proctor, Robert H.; Stewart, Jane E.; Snook, M. E.

doi:10.1371/journal.pone.0147486

Cited by 43 publications

(55 citation statements)

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“…Many of the clusters observed in this study have discontinuous phylogenetic distributions consistent with evolutionary scenarios such as vertical inheritance coupled with extensive loss, convergence, duplication, or horizontal gene transfer (HGT). HGT of MGCs is predicted to be associated with rapid adaptive changes to phenotypes, including increased capacity for host colonization [10,11] and nutrient acquisition [60]. For example, MGCs in bacteria are frequently dispersed by HGT among species inhabiting the same environment or host [1].…”

Section: Candidate Phenlypropanoid Degradation Mgcs Are Found At Overmentioning

confidence: 99%

“…Fungal genomes contain many metabolic gene clusters (MGCs) composed of genes encoding enzymes, transporters, and regulators that participate in specialized metabolic processes such as nutrient acquisition, competition, and defense [9]. Although MGCs are far more rare in fungi compared with bacteria, fungal MGCs exhibit similarly sparse distributions among distantly related species with overlapping niches [10][11][12]. This ecological pattern of distribution suggests that conserved combinations of genes may be signatures of ecological selection in fungal genomes.…”

Section: Introductionmentioning

confidence: 99%

“…Fungal MGCs encoding specialized or secondary metabolite (SM) production have been studied extensively [13] and more recently, several reports suggest that MGCs also encode adaptations to degrade plant SMs [11,12,[14][15][16]. Plant SMs mediate important biotic and abiotic interactions, including the exclusion of fungal pathogens and the rates of nutrient cycling long after the plant has died.…”

Section: Introductionmentioning

confidence: 99%

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Specialized plant biochemistry drives gene clustering in fungi

Gluck‐Thaler

Slot

2018

The ISME Journal

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The fitness and evolution of prokaryotes and eukaryotes are affected by the organization of their genomes. In particular, the physical clustering of genes can coordinate gene expression and can prevent the breakup of co-adapted alleles. Although clustering may thus result from selection for phenotype optimization and persistence, the impact of environmental selection pressures on eukaryotic genome organization has rarely been systematically explored. Here, we investigated the organization of fungal genes involved in the degradation of phenylpropanoids, a class of plant-produced secondary metabolites that mediate many ecological interactions between plants and fungi. Using a novel gene cluster detection method, we identified 1110 gene clusters and many conserved combinations of clusters in a diverse set of fungi. We demonstrate that congruence in genome organization over small spatial scales is often associated with similarities in ecological lifestyle. Additionally, we find that while clusters are often structured as independent modules with little overlap in content, certain gene families merge multiple modules into a common network, suggesting they are important components of phenylpropanoid degradation strategies. Together, our results suggest that phenylpropanoids have repeatedly selected for gene clustering in fungi, and highlight the interplay between genome organization and ecological evolution in this ancient eukaryotic lineage.

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Section: Candidate Phenlypropanoid Degradation Mgcs Are Found At Overmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Specialized plant biochemistry drives gene clustering in fungi

Gluck‐Thaler

Slot

2018

The ISME Journal

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“…Among eukaryotes, fungi possess some of the most highly clustered genomes (Slot, ). Fungal MGCs that synthesize SMs are well studied, and, increasingly, fungal mechanisms to degrade/assimilate plant SMs are also found encoded in clusters (Glenn et al, ; Gluck‐Thaler & Slot, ; Kettle et al, ). For example, a fungal MGC encoding a putative pathway for the degradation of plant‐produced stilbene molecules was recently reported by Greene, McGary, Rokas, and Slot ().…”

Section: Introductionmentioning

confidence: 99%

Fungal adaptation to plant defences through convergent assembly of metabolic modules

2018

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The ongoing diversification of plant defence compounds exerts dynamic selection pressures on the microorganisms that colonize plant tissues. Evolutionary processes that generate resistance towards these compounds increase microbial fitness by giving access to plant resources and increasing pathogen virulence. These processes entail sequence‐based mechanisms that result in adaptive gene functions, and combinatorial mechanisms that result in novel syntheses of existing gene functions. However, the priority and interactions among these processes in adaptive resistance remain poorly understood. Using a combination of molecular genetic and computational approaches, we investigated the contributions of sequence‐based and combinatorial processes to the evolution of fungal metabolic gene clusters encoding stilbene cleavage oxygenases (SCOs), which catalyse the degradation of biphenolic plant defence compounds known as stilbenes into monophenolic molecules. We present phylogenetic evidence of convergent assembly among three distinct types of SCO gene clusters containing alternate combinations of phenolic catabolism. Multiple evolutionary transitions between different cluster types suggest recurrent selection for distinct gene assemblages. By comparison, we found that the substrate specificities of heterologously expressed SCO enzymes encoded in different clusters types were all limited to stilbenes and related molecules with a 4′‐OH group, and differed modestly in substrate range and activity under the experimental conditions. Together, this work suggests a primary role for genome structural rearrangement, and the importance of enzyme modularity, in promoting fungal metabolic adaptation to plant defence chemistry.

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“…Among eukaryotes, fungi possess some of the most highly clustered genomes (Slot 2017). Fungal MGCs that synthesize SMs are well studied, and increasingly, fungal mechanisms to degrade/assimilate plant SMs are also found encoded in clusters (Kettle et al 2015; Glenn et al 2016; Gluck-Thaler & Slot 2018). For example, a fungal MGC encoding a putative pathway for the degradation of plant-produced stilbene molecules was recently reported by (Greene et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Fungal adaptation to plant defenses through convergent assembly of metabolic modules

Gluck‐Thaler

Vijayakumar

Slot

2018

Preprint

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25The ongoing diversification of plant defense compounds exerts dynamic selection pressures on 26 the microorganisms that colonize plant tissues. Evolutionary processes that generate resistance 27 towards these compounds increase microbial fitness by giving access to plant resources and 28 increasing pathogen virulence. These processes entail sequence-based mechanisms that result in 29 adaptive gene functions, and combinatorial mechanisms that result in novel syntheses of existing 30 gene functions. However, the priority and interactions among these processes in adaptive 31 resistance remains poorly understood. Using a combination of molecular genetic and 32 computational approaches, we investigated the contributions of sequence-based and 33 combinatorial processes to the evolution of fungal metabolic gene clusters encoding stilbene 34 cleavage oxygenases (SCOs), which catalyze the degradation of biphenolic plant defense 35 compounds known as stilbenes into monophenolic molecules. We present phylogenetic evidence 36 of convergent assembly among three distinct types of SCO gene clusters containing alternate 37 combinations of phenolic catabolism. Multiple evolutionary transitions between different cluster 38 types suggest recurrent selection for distinct gene assemblages. By comparison, we found that 39 the substrate specificities of heterologously expressed SCO enzymes encoded in different 40 clusters types were all limited to stilbenes and related molecules with a 4'-OH group, and 41 differed modestly in substrate range and activity under the experimental conditions. Together, 42 this work suggests a primary role for genome structural rearrangement, and the importance of 43 enzyme modularity, in promoting fungal metabolic adaptation to plant defense chemistry. 44 45 106 remodeling can operate independently of sequence-based evolution. We analyzed the substrate 107 specificities of four heterologously expressed SCOs from different cluster types and unclustered 108 genomic regions, and found evidence for broad conservation of substrate specificity in both 109 unclustered and clustered SCOs, with only modest variation in the substrate specificity of SCOs 110 found in alternate cluster types. Conversely, we found evidence for multiple independent origins 111 of and repeated transitions between different types of sco clusters, consistent with selection 112 acting upon recurrent combinations of enzyme-encoding genes. These results suggest that the 113 6 reorganization of sco clusters may underpin adaptive shifts in stilbene degradation pathways, 114 while changes in enzymatic function may play a secondary role. 115 116 Methods 117 sco cluster retrieval and annotation 118 sco clusters were identified in publicly available genomes of 550 fungi (Table S1) as previously 119 described (Gluck-Thaler & Slot 2018). Briefly, all hits to a previously functionally characterized 120 SCO amino acid query (accession: EAA32528.1) were retrieved from predicted proteomes using 121 BLASTp from the BLAST suite v.2.2.25+ (Altschul et al....

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

Cited by 43 publications

References 45 publications

Specialized plant biochemistry drives gene clustering in fungi

Specialized plant biochemistry drives gene clustering in fungi

Fungal adaptation to plant defences through convergent assembly of metabolic modules

Fungal adaptation to plant defenses through convergent assembly of metabolic modules

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