Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp

Detalhes bibliográficos
Autor(a) principal: Pinto, Ciro P.G. [UNESP]
Data de Publicação: 2022
Outros Autores: Walker, Andrew A., Robinson, Samuel D., King, Glenn F., Rossi, Guilherme D. [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1016/j.jinsphys.2022.104395
http://hdl.handle.net/11449/223796
Resumo: Parasitoid wasps have evolved sophisticated mechanisms of host regulation that establish a favorable environment for the development of immature parasitoids. While maternal venom and symbiotic virus-like particles are well-known mechanisms of host regulation, another less-studied mechanism is the secretion of host regulation factors by cells called teratocytes, extra-embryonic cells released during parasitoid larval eclosion. Consequently, identification and characterization of teratocyte secretory products has not been reported in detail for any parasitoid wasp. We aimed to analyze teratocyte secretory products released into hemolymph of the larval sugarcane borer Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae) by its biological control agent, the koinobiont endoparasitoid wasp Cotesia flavipes Cameron, 1891 (Hymenoptera: Braconidae). Teratocytes were released upon eclosion of parasitoid larvae four days after parasitization (DAP) and increased in number and size until six DAP. Total D. saccharalis hemocyte viability was reduced immediately after parasitization until DAP 2, while total hemocyte count was lower from the third DAP, and phenoloxidase and lysozyme activity were disrupted compared to non-parasitized controls. To examine the secretory products of teratocytes, we generated a teratocyte transcriptome and compared its in silico translated open reading frames to mass spectra obtained from hemolymph from parasitized and unparasitized hosts. This led to the identification of 57 polypeptides secreted by teratocytes, the abundance of which we tracked over 0–10 DAP. Abundant teratocyte products included proteins similar to bracovirus proteins and multiple disulfide-rich peptides. Most teratocyte products accumulated in hemolymph, reaching their highest concentrations immediately before parasitoid pupation. Our results provide insights into host regulation by teratocytes and reveal molecules that may be useful in biotechnology.
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spelling Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid waspBiological controlDefensinImmune systemLysozymePeptidePhenoloxidaseParasitoid wasps have evolved sophisticated mechanisms of host regulation that establish a favorable environment for the development of immature parasitoids. While maternal venom and symbiotic virus-like particles are well-known mechanisms of host regulation, another less-studied mechanism is the secretion of host regulation factors by cells called teratocytes, extra-embryonic cells released during parasitoid larval eclosion. Consequently, identification and characterization of teratocyte secretory products has not been reported in detail for any parasitoid wasp. We aimed to analyze teratocyte secretory products released into hemolymph of the larval sugarcane borer Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae) by its biological control agent, the koinobiont endoparasitoid wasp Cotesia flavipes Cameron, 1891 (Hymenoptera: Braconidae). Teratocytes were released upon eclosion of parasitoid larvae four days after parasitization (DAP) and increased in number and size until six DAP. Total D. saccharalis hemocyte viability was reduced immediately after parasitization until DAP 2, while total hemocyte count was lower from the third DAP, and phenoloxidase and lysozyme activity were disrupted compared to non-parasitized controls. To examine the secretory products of teratocytes, we generated a teratocyte transcriptome and compared its in silico translated open reading frames to mass spectra obtained from hemolymph from parasitized and unparasitized hosts. This led to the identification of 57 polypeptides secreted by teratocytes, the abundance of which we tracked over 0–10 DAP. Abundant teratocyte products included proteins similar to bracovirus proteins and multiple disulfide-rich peptides. Most teratocyte products accumulated in hemolymph, reaching their highest concentrations immediately before parasitoid pupation. Our results provide insights into host regulation by teratocytes and reveal molecules that may be useful in biotechnology.School of Agricultural and Veterinarian Sciences São Paulo State University (UNESP)Institute for Molecular Bioscience The University of QueenslandAustralian Research Council Centre of Excellence for Innovations in Peptide and Protein Science The University of QueenslandSchool of Agricultural and Veterinarian Sciences São Paulo State University (UNESP)Universidade Estadual Paulista (UNESP)The University of QueenslandPinto, Ciro P.G. [UNESP]Walker, Andrew A.Robinson, Samuel D.King, Glenn F.Rossi, Guilherme D. [UNESP]2022-04-28T19:53:02Z2022-04-28T19:53:02Z2022-05-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1016/j.jinsphys.2022.104395Journal of Insect Physiology, v. 139.0022-1910http://hdl.handle.net/11449/22379610.1016/j.jinsphys.2022.1043952-s2.0-85127870806Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengJournal of Insect Physiologyinfo:eu-repo/semantics/openAccess2022-04-28T19:53:02Zoai:repositorio.unesp.br:11449/223796Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T22:28:02.382921Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
title Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
spellingShingle Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
Pinto, Ciro P.G. [UNESP]
Biological control
Defensin
Immune system
Lysozyme
Peptide
Phenoloxidase
title_short Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
title_full Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
title_fullStr Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
title_full_unstemmed Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
title_sort Proteotranscriptomics reveals the secretory dynamics of teratocytes, regulators of parasitization by an endoparasitoid wasp
author Pinto, Ciro P.G. [UNESP]
author_facet Pinto, Ciro P.G. [UNESP]
Walker, Andrew A.
Robinson, Samuel D.
King, Glenn F.
Rossi, Guilherme D. [UNESP]
author_role author
author2 Walker, Andrew A.
Robinson, Samuel D.
King, Glenn F.
Rossi, Guilherme D. [UNESP]
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (UNESP)
The University of Queensland
dc.contributor.author.fl_str_mv Pinto, Ciro P.G. [UNESP]
Walker, Andrew A.
Robinson, Samuel D.
King, Glenn F.
Rossi, Guilherme D. [UNESP]
dc.subject.por.fl_str_mv Biological control
Defensin
Immune system
Lysozyme
Peptide
Phenoloxidase
topic Biological control
Defensin
Immune system
Lysozyme
Peptide
Phenoloxidase
description Parasitoid wasps have evolved sophisticated mechanisms of host regulation that establish a favorable environment for the development of immature parasitoids. While maternal venom and symbiotic virus-like particles are well-known mechanisms of host regulation, another less-studied mechanism is the secretion of host regulation factors by cells called teratocytes, extra-embryonic cells released during parasitoid larval eclosion. Consequently, identification and characterization of teratocyte secretory products has not been reported in detail for any parasitoid wasp. We aimed to analyze teratocyte secretory products released into hemolymph of the larval sugarcane borer Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae) by its biological control agent, the koinobiont endoparasitoid wasp Cotesia flavipes Cameron, 1891 (Hymenoptera: Braconidae). Teratocytes were released upon eclosion of parasitoid larvae four days after parasitization (DAP) and increased in number and size until six DAP. Total D. saccharalis hemocyte viability was reduced immediately after parasitization until DAP 2, while total hemocyte count was lower from the third DAP, and phenoloxidase and lysozyme activity were disrupted compared to non-parasitized controls. To examine the secretory products of teratocytes, we generated a teratocyte transcriptome and compared its in silico translated open reading frames to mass spectra obtained from hemolymph from parasitized and unparasitized hosts. This led to the identification of 57 polypeptides secreted by teratocytes, the abundance of which we tracked over 0–10 DAP. Abundant teratocyte products included proteins similar to bracovirus proteins and multiple disulfide-rich peptides. Most teratocyte products accumulated in hemolymph, reaching their highest concentrations immediately before parasitoid pupation. Our results provide insights into host regulation by teratocytes and reveal molecules that may be useful in biotechnology.
publishDate 2022
dc.date.none.fl_str_mv 2022-04-28T19:53:02Z
2022-04-28T19:53:02Z
2022-05-01
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1016/j.jinsphys.2022.104395
Journal of Insect Physiology, v. 139.
0022-1910
http://hdl.handle.net/11449/223796
10.1016/j.jinsphys.2022.104395
2-s2.0-85127870806
url http://dx.doi.org/10.1016/j.jinsphys.2022.104395
http://hdl.handle.net/11449/223796
identifier_str_mv Journal of Insect Physiology, v. 139.
0022-1910
10.1016/j.jinsphys.2022.104395
2-s2.0-85127870806
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Journal of Insect Physiology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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