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

BACKGROUND: Stick 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...

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Autores principales: Shelomi, Matan, Jasper, W Cameron, Atallah, Joel, Kimsey, Lynn S, Johnson, Brian R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4221708/
https://www.ncbi.nlm.nih.gov/pubmed/25331961
http://dx.doi.org/10.1186/1471-2164-15-917
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author Shelomi, Matan
Jasper, W Cameron
Atallah, Joel
Kimsey, Lynn S
Johnson, Brian R
author_facet Shelomi, Matan
Jasper, W Cameron
Atallah, Joel
Kimsey, Lynn S
Johnson, Brian R
author_sort Shelomi, Matan
collection PubMed
description BACKGROUND: Stick 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. RESULTS: We 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. CONCLUSIONS: We 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 MATERIAL: The 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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spelling pubmed-42217082014-11-07 Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut Shelomi, Matan Jasper, W Cameron Atallah, Joel Kimsey, Lynn S Johnson, Brian R BMC Genomics Research Article BACKGROUND: Stick 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. RESULTS: We 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. CONCLUSIONS: We 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 MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-917) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-21 /pmc/articles/PMC4221708/ /pubmed/25331961 http://dx.doi.org/10.1186/1471-2164-15-917 Text en © Shelomi et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Shelomi, Matan
Jasper, W Cameron
Atallah, Joel
Kimsey, Lynn S
Johnson, Brian R
Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
title Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
title_full Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
title_fullStr Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
title_full_unstemmed Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
title_short Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
title_sort differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (phasmatodea) midgut
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4221708/
https://www.ncbi.nlm.nih.gov/pubmed/25331961
http://dx.doi.org/10.1186/1471-2164-15-917
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