Ancestral gene fusion in cellobiose dehydrogenases reflects a specific evolution of GMC oxidoreductases in fungi

Zámocký, Marcel; Hällberg, B. Martin; Ludwig, Roland; Divne, Christina; Haltrich, Dietmar

doi:10.1016/j.gene.2004.04.025

Cited by 84 publications

(74 citation statements)

References 30 publications

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“…Threedimensional crystal structures have previously been solved for some members of this enzyme family and have shown the presence of a conserved p-hydroxybenzoate hydroxylase-like fold (36 -40). Despite the structural and sequence similarities, the members of the GMC oxidoreductase family catalyze surprisingly diverse reactions (41), suggesting a high variability within the catalytic centers that are mainly formed by the C-terminal region of the sequence, which has been shown to contain the substrate-binding domain (34). Most of the GMC-like sequences known to date have arisen from recent genome projects, so there is no information about their natural substrates.…”

Section: Discussionmentioning

confidence: 99%

Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles

Michalski

Mohagheghi

Nimtz

et al. 2008

Journal of Biological Chemistry

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Salicyl alcohol oxidase is an extracellular enzyme that occurs in glandular reservoirs of chrysomelid leaf beetle larvae and catalyzes the formation of salicylaldehyde, a volatile deterrent used by the larvae against predators. Salicyl alcohol is the hydrolysis product of salicin, a plant-derived precursor taken up by the beetle larvae from the leaves of willow and poplar trees. The cDNA encoding salicyl alcohol oxidase from two related species Chrysomela tremulae and Chrysomela populi has been identified, cloned, and expressed in an active form in Escherichia coli. The open reading frame of 623 amino acids begins in both enzymes with an N-terminal signal peptide of 21 amino acids. Sequence comparison has revealed that salicyl alcohol oxidase belongs to the family of glucose-methanol-choline oxidoreductase-like sequences with mostly unknown function. Enzymes of this family share similar overall structure with an essentially identical FAD-binding site but possess different catalytic activities. The data suggest that salicyl alcohol oxidase, essential for the activation of the plant-derived precursor salicin, was originally recruited from an oxidase involved in the autogenous biosynthesis of iridoid monoterpenes and found in related chrysomelid leaf beetle species.

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Section: Discussionmentioning

confidence: 99%

Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles

Michalski

Mohagheghi

Nimtz

et al. 2008

Journal of Biological Chemistry

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“…Cellobiose dehydrogenase (EC 1.1.99.18) is an enzyme that oxidizes cellobiose to cellobiolactone in the presence of an electron acceptor, such as cytochrome c, dichlorophenol-indophenol, or ferricyanide, producing cellobiono-1,5-lactone and a reduced acceptor (131,132). Cellobiose dehydrogenases are well studied in white and brown rot and plant-pathogenic as well as composting fungi from the dikaryotic phyla Basidiomycota and Ascomycota under cellulolytic culture conditions (133).…”

Section: Cellulasesmentioning

confidence: 99%

Genomics Review of Holocellulose Deconstruction by Aspergilli

Segato

Damásio

Lucas

et al. 2014

Microbiol Mol Biol Rev

115

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SUMMARY Biomass is constructed of dense recalcitrant polymeric materials: proteins, lignin, and holocellulose, a fraction constituting fibrous cellulose wrapped in hemicellulose-pectin. Bacteria and fungi are abundant in soil and forest floors, actively recycling biomass mainly by extracting sugars from holocellulose degradation. Here we review the genome-wide contents of seven Aspergillus species and unravel hundreds of gene models encoding holocellulose-degrading enzymes. Numerous apparent gene duplications followed functional evolution, grouping similar genes into smaller coherent functional families according to specialized structural features, domain organization, biochemical activity, and genus genome distribution. Aspergilli contain about 37 cellulase gene models, clustered in two mechanistic categories: 27 hydrolyze and 10 oxidize glycosidic bonds. Within the oxidative enzymes, we found two cellobiose dehydrogenases that produce oxygen radicals utilized by eight lytic polysaccharide monooxygenases that oxidize glycosidic linkages, breaking crystalline cellulose chains and making them accessible to hydrolytic enzymes. Among the hydrolases, six cellobiohydrolases with a tunnel-like structural fold embrace single crystalline cellulose chains and cooperate at nonreducing or reducing end termini, splitting off cellobiose. Five endoglucanases group into four structural families and interact randomly and internally with cellulose through an open cleft catalytic domain, and finally, seven extracellular β-glucosidases cleave cellobiose and related oligomers into glucose. Aspergilli contain, on average, 30 hemicellulase and 7 accessory gene models, distributed among 9 distinct functional categories: the backbone-attacking enzymes xylanase, mannosidase, arabinase, and xyloglucanase, the short-side-chain-removing enzymes xylan α-1,2-glucuronidase, arabinofuranosidase, and xylosidase, and the accessory enzymes acetyl xylan and feruloyl esterases.

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“…These SAOs belong to the glucose-methanol-choline (GMC) oxidoreductase multi-gene family [22,23] and convert salicyl alcohol into salicylaldehyde [20]. Comparative genome analyses show that the GMC oxidoreductase family harbours genes, most of which are in a cluster and unique with respect to their expansion in insects [24][25][26]. Phylogenetic analyses of the functional SAOs from salicin-sequestering Chrysomelina sensu stricto strongly support the SAOs' common ancestry in the GMCi clade [16] irrespective of the evolutionary affiliation of the corresponding beetle species [5].…”

Section: Introductionmentioning

confidence: 99%

Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve

et al. 2014

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Larvae of the leaf beetle subtribe Chrysomelina sensu stricto repel their enemies by displaying glandular secretions that contain defensive compounds. These repellents can be produced either de novo (iridoids) or by using plant-derived precursors (e.g. salicylaldehyde). The autonomous production of iridoids, as in Phaedon cochleariae, is the ancestral chrysomeline chemical defence and predates the evolution of salicylaldehyde-based defence. Both biosynthesis strategies include an oxidative step of an alcohol intermediate. In salicylaldehyde-producing species, this step is catalysed by salicyl alcohol oxidases (SAOs) of the glucose-methanol-choline (GMC) oxidoreductase superfamily, but the enzyme oxidizing the iridoid precursor is unknown. Here, we show by in vitro as well as in vivo experiments that P. cochleariae also uses an oxidase from the GMC superfamily for defensive purposes. However, our phylogenetic analysis of chrysomeline GMC oxidoreductases revealed that the oxidase of the iridoid pathway originated from a GMC clade different from that of the SAOs. Thus, the evolution of a host-independent chemical defence followed by a shift to a host-dependent chemical defence in chrysomeline beetles coincided with the utilization of genes from different GMC subfamilies. These findings illustrate the importance of the GMC multi-gene family for adaptive processes in plant-insect interactions.

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Ancestral gene fusion in cellobiose dehydrogenases reflects a specific evolution of GMC oxidoreductases in fungi

Cited by 84 publications

References 30 publications

Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles

Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles

Genomics Review of Holocellulose Deconstruction by Aspergilli

Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve

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