Immunity or Digestion

Pauchet, Yannick; Freitak, Dalial; Heidel‐Fischer, Hanna M.; Heckel, David G.; Vogel, Heiko

doi:10.1074/jbc.m806204200

Cited by 85 publications

(46 citation statements)

References 39 publications

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“…We also found transcripts encoding beta-1,3-glucanase (EC:3.2.1.39), a polysaccharide-degrading enzyme family known mostly from Lepidoptera larval midguts and expressed in response to feeding on a diet containing bacteria [74]. These four enzymes (cellulases, cellobiases, pectinases, and beta-1,3-glucanases) were used in the manual annotations.…”

Section: Resultsmentioning

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: Resultsmentioning

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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“…Several such proteins have been identified in moths and butterflies (Fabrick et al, 2004). These proteins are usually isolated from hemolymph, but have also been found in the saliva and digestive tracts of other insects (Pauchet et al, 2009). REPAT and hemolin are Lepidopteran specific immune proteins that have shown increased expression in response to pathogen infection in caterpillars of several species (Hern andez-Rodríguez et al, 2009;Terenius et al, 2009;Yamamoto et al, 1999).…”

Section: Immune Functionmentioning

confidence: 99%

Pollen feeding proteomics: Salivary proteins of the passion flower butterfly, Heliconius melpomene

Harpel

Cullen

Ott

et al. 2015

Insect Biochemistry and Molecular Biology

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While most adult Lepidoptera use flower nectar as their primary food source, butterflies in the genus Heliconius have evolved the novel ability to acquire amino acids from consuming pollen. Heliconius butterflies collect pollen on their proboscis, moisten the pollen with saliva, and use a combination of mechanical disruption and chemical degradation to release free amino acids that are subsequently re-ingested in the saliva. Little is known about the molecular mechanisms of this complex pollen feeding adaptation. Here we report an initial shotgun proteomic analysis of saliva from Heliconius melpomene. Results from liquid-chromatography tandem mass-spectrometry confidently identified 31 salivary proteins, most of which contained predicted signal peptides, consistent with extracellular secretion. Further bioinformatic annotation of these salivary proteins indicated the presence of four distinct functional classes: proteolysis (10 proteins), carbohydrate hydrolysis (5), immunity (6), and "housekeeping" (4). Additionally, six proteins could not be functionally annotated beyond containing a predicted signal sequence. The presence of several salivary proteases is consistent with previous demonstrations that Heliconius saliva has proteolytic capacity. It is likely that these proteins play a key role in generating free amino acids during pollen digestion. The identification of proteins functioning in carbohydrate hydrolysis is consistent with Heliconius butterflies consuming nectar, like other lepidopterans, as well as pollen. Immune-related proteins in saliva are also expected, given that ingestion of pathogens is a likely route to infection. The few "housekeeping" proteins are likely not true salivary proteins and reflect a modest level of contamination that occurred during saliva collection. Among the unannotated proteins were two sets of paralogs, each seemingly the result of a relatively recent tandem duplication. These results offer a first glimpse into the molecular foundation of Heliconius pollen feeding and provide a substantial advance towards comprehensively understanding this striking evolutionary novelty.

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“…7). The insect β-glucan binding protein lacks the catalytic amino acids present in the β-1,3-glucanases (Pauchet et al, 2009). The two genes are related but evolutionary distinct.…”

Section: Phylogenetic Analysis Of Sequencesmentioning

confidence: 99%

“…The β-1,3-glucanase may work like lysozyme by hydrolysing the β-1,3-glucans within cell walls of fungi and bacteria to potentially render them inactive. Indeed, the β-1,3-glucanases secreted into the midgut by insects such Tenebrio and lepidopteran, Helicoverpa armigera can hydrolyse the cell walls of these organisms (Genta et al, 2009;Pauchet et al, 2009). As described for the GHF16 β-glucan binding proteins in the haemolymph, the GFH16 protein in the digestive fluid may also bind to the β-1,3-glucans in the cell walls of micro-organisms and stimulate the prophenol oxidase system to activate a humoral immune response (Lee et al, 2000;Sritunyalucksana and Söderhäll, 2000;Amparyup et al, 2012).…”

Section: Immune Proteinmentioning

confidence: 99%

“…This may have occurred in insects, with the protein initially being a β-1,3-glucanase. The protein expressed within the haemolymph may have then lost the catalytic amino acids and evolved into a separate β-glucan binding protein whose function is to amplify the signal of a potentially pathogenic micro-organism (Pauchet et al, 2009). Given these hypotheses, the β-1,3-glucanase from species that do not consume significant amounts of β-1,3-glucans needs to be isolated and characterised in terms of its immune function; that is, its potential to hydrolyse the cell walls of micro-organisms and its ability to activate the prophenol oxidase system in both the haemolymph and digestive fluid.…”

Section: Evolutionary Relationship Of the β-13-glucanases And β-Glucmentioning

confidence: 99%

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A glycosyl hydrolase family 16 gene is responsible for the endogenous production of β-1,3-glucanases within decapod crustaceans

Linton

Cameron

Gray

et al. 2015

Gene

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To identify the gene responsible for the production of a β-1,3-glucanase (laminarinase) within crustacea, a glycosyl hydrolase family 16 (GHF16) gene was sequenced from the midgut glands of the gecarcinid land crab, Gecarcoidea natalis and the freshwater crayfish, Cherax destructor. An open reading frame of 1098 bp for G. natalis and 1095 bp for C. destructor was sequenced from cDNA. For G. natalis and C. destructor respectively, this encoded putative proteins of 365 and 364 amino acids with molecular masses of 41.4 and 41.5 kDa. mRNA for an identical GHF16 protein was also expressed in the haemolymph of C. destructor. These putative proteins contained binding and catalytic domains that are characteristic of a β-1,3-glucanase from glycosyl hydrolase family 16. The amino acid sequences of two short 8-9 amino acid residue peptides from a previously purified β-1,3-glucanase from G. natalis matched exactly that of the putative protein sequence. This plus the molecular masses of the putative proteins matching that of the purified proteins strongly suggests that the sequences obtained encode for a catalytically active β-1,3-glucanase. A glycosyl hydrolase family 16 cDNA was also partially sequenced from the midgut glands of other amphibious (Mictyris platycheles and Paragrapsus laevis) and terrestrial decapod species (Coenobita rugosus, Coenobita perlatus, Coenobita brevimanus and Birgus latro) to confirm that the gene is widely expressed within this group. There are three possible hypothesised functions and thus evolutionary routes for the β-1,3-glucanase: 1) a digestive enzyme which hydrolyses β-1,3-glucans, 2) an enzyme which cleaves β-1,3-glycosidic bonds within cell walls to release cell contents or 3) an immune protein which can hydrolyse the cell walls of potentially pathogenic micro-organisms.

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Immunity or Digestion

Cited by 85 publications

References 39 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

Pollen feeding proteomics: Salivary proteins of the passion flower butterfly, Heliconius melpomene

A glycosyl hydrolase family 16 gene is responsible for the endogenous production of β-1,3-glucanases within decapod crustaceans

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