Identification and characterization of plant cell wall degrading enzymes from three glycoside hydrolase families in the cerambycid beetle Apriona japonica

Pauchet, Yannick; Kirsch, Roy; Giraud, Sandra; Vogel, Heiko; Heckel, David G.

doi:10.1016/j.ibmb.2014.03.004

Cited by 61 publications

(88 citation statements)

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“…However, because some isotigs were truncated at the 3’ or 5’ end, the possibility exists that certain transcripts represent different ends of a single gene. Future work using RACE-PCR from primers based on the transcripts identified here would produce full-length cDNA sequences that will determine which transcripts represent unique genes and which are fragments, Such genes could then be expressed into insect cell cultures for use in downstream enzymatic activity assays [85]. …”

Section: Discussionmentioning

confidence: 99%

Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut

et al. 2014

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BackgroundStick and leaf insects (Phasmatodea) are an exclusively leaf-feeding order of insects with no record of omnivory, unlike other “herbivorous” Polyneoptera. They represent an ideal system for investigating the adaptations necessary for obligate folivory, including plant cell wall degrading enzymes (PCWDEs). However, their physiology and internal anatomy is poorly understood, with limited genomic resources available.ResultsWe de novo assembled transcriptomes for the anterior and posterior midguts of six diverse Phasmatodea species, with RNA-Seq on one exemplar species, Peruphasma schultei. The latter’s assembly yielded >100,000 transcripts, with over 4000 transcripts uniquely or more highly expressed in specific midgut sections. Two to three dozen PCWDE encoding gene families, including cellulases and pectinases, were differentially expressed in the anterior midgut. These genes were also found in genomic DNA from phasmid brain tissue, suggesting endogenous production. Sequence alignments revealed catalytic sites on most PCWDE transcripts. While most phasmid PCWDE genes showed homology with those of other insects, the pectinases were homologous to bacterial genes.ConclusionsWe identified a large and diverse PCWDE repertoire endogenous to the phasmids. If these expressed genes are translated into active enzymes, then phasmids can theoretically break plant cell walls into their monomer components independently of microbial symbionts. The differential gene expression between the two midgut sections provides the first molecular hints as to their function in living phasmids. Our work expands the resources available for industrial applications of animal-derived PCWDEs, and facilitates evolutionary analysis of lower Polyneopteran digestive enzymes, including the pectinases whose origin in Phasmatodea may have been a horizontal transfer event from bacteria.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-917) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut

et al. 2014

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“…Successful feeding on woody plants therefore requires specialized metabolic adaptations. The genomes of A. glabripennis and certain other phytophagous beetles are known to contain genes encoding plant cell wall degrading enzymes (PCWDEs) [7–9]. PCWDEs degrade cellulose, hemicellulose, or pectin (the main polysaccharide networks in plant cell walls), liberating sugars, minerals, and other nutrients from woody plant tissues.…”

Section: Introductionmentioning

confidence: 99%

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

et al. 2016

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BackgroundRelatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.ResultsThe Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.ConclusionsAmplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users.

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“…GH5 cellulases from longhorn beetles form a monophyletic branch in the phylogenetic tree, indicating that the GH5 cellulases share a common ancestor. Several Lamiinae longhorn beetles contain relatively large numbers of GH5 cellulase copies [28,36]. This situation is special and has seldom been reported in insects.…”

Section: Discussionmentioning

confidence: 99%

“…The expansion of GH5 cellulases in longhorn beetles, including M. myops, is therefore a rather unique phenomenon in insects. Recently, GH5 cellulases have also been identified, using transcriptomic methods, in the Cerambycid species A. glabripennis [28] and Apriona japonica [36]. It is well known that longhorn beetle larvae can ingest wood materials and therefore cellulose is the main carbon source for their metabolism and growth.…”

Section: Discussionmentioning

confidence: 99%

Endogenous cellulolytic enzyme systems in the longhorn beetle <italic>Mesosa myops</italic> (Insecta: Coleoptera) studied by transcriptomic analysis

Liu¹,

Song²,

Teng³

et al. 2015

ABBS

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The Cerambycidae (longhorn beetle) is a large family of Coleoptera with xylophagous feeding habits. Cellulose digestion plays an important role in these wood-feeding insects. In this study, transcriptomic technology was used to obtain one glycoside hydrolase family 45 (GH45) cellulase and seven GH5 cellulases from Mesosa myops, a typical longhorn beetle. Analyses of expression dynamics and evolutionary relationships provided a complete description of the cellulolytic system. The expression dynamics related to individual development indicated that endogenous GH45 and GH5 cellulases dominate cellulose digestion in M. myops. Evolutionary analyses suggested that GH45 cellulase gene is a general gene in the Coleoptera Suborder Polyphaga. Evolutionary analyses also indicated that the GH5 cellulase group in Lamiinae longhorn beetles is closely associated with wood feeding. This study demonstrated that there is a complex endogenous cellulolytic system in M. myops that is dominated by cellulases belonging to two glycoside hydrolase families.

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Identification and characterization of plant cell wall degrading enzymes from three glycoside hydrolase families in the cerambycid beetle Apriona japonica

Cited by 61 publications

References 37 publications

Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut

Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

Endogenous cellulolytic enzyme systems in the longhorn beetle <italic>Mesosa myops</italic> (Insecta: Coleoptera) studied by transcriptomic analysis

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Identification and characterization of plant cell wall degrading enzymes from three glycoside hydrolase families in the cerambycid beetle Apriona japonica

Cited by 61 publications

References 37 publications

Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut

Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

Endogenous cellulolytic enzyme systems in the longhorn beetle &lt;italic&gt;Mesosa myops&lt;/italic&gt; (Insecta: Coleoptera) studied by transcriptomic analysis

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Endogenous cellulolytic enzyme systems in the longhorn beetle <italic>Mesosa myops</italic> (Insecta: Coleoptera) studied by transcriptomic analysis