The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation

Autores
Dreon, Marcos Sebastián; Ituarte, Santiago; Heras, Horacio
Año de publicación
2010
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background: Fieldwork has thoroughly established that most eggs are intensely predated. Among the few exceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which have virtually no predators. Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuous reddish coloration. The nature of the defense however, was not clear, except for a screening for defenses that identified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinase inhibitor (PI) whose role to protect against pathogens was taken for granted, according to the prevailing assumption. Through biochemical, biophysical and feeding experiments we studied the proteinase inhibitor function of ovorubin in egg defenses. Methodology/Principal Findings: Mass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinase inhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering (SAXS) and crosslinking studies but, in contrast to the classical assumption, it does not prevent bacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis. Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in rats indicating that this highly stable PI is capable of surviving passage through the gastrointestinal tract in a biologically active form. Conclusions: To our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestive protease of potential predators, limiting predator's ability to digest egg nutrients. This role has not been reported in the animal kingdom but it is similar to plant defenses against herbivory. Further, this would be the only defense model with no tradeoffs between conspicuousness and noxiousness by encoding into the same molecule both the aposematic warning signal and an antinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probably unpalatable factors would explain the near absence of predators, opening new perspectives in the study of the evolution and ecology of egg defensive strategies.
Facultad de Ciencias Naturales y Museo
Materia
Ciencias Naturales
Bioquímica
Caracoles
predadores
Inhibidores de Serina Proteinasa
embriones
nutrientes
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by/2.5/ar/
Repositorio
SEDICI (UNLP)
Institución
Universidad Nacional de La Plata
OAI Identificador
oai:sedici.unlp.edu.ar:10915/29607

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network_name_str SEDICI (UNLP)
spelling The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predationDreon, Marcos SebastiánItuarte, SantiagoHeras, HoracioCiencias NaturalesBioquímicaCaracolespredadoresInhibidores de Serina ProteinasaembrionesnutrientesBackground: Fieldwork has thoroughly established that most eggs are intensely predated. Among the few exceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which have virtually no predators. Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuous reddish coloration. The nature of the defense however, was not clear, except for a screening for defenses that identified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinase inhibitor (PI) whose role to protect against pathogens was taken for granted, according to the prevailing assumption. Through biochemical, biophysical and feeding experiments we studied the proteinase inhibitor function of ovorubin in egg defenses. Methodology/Principal Findings: Mass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinase inhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering (SAXS) and crosslinking studies but, in contrast to the classical assumption, it does not prevent bacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis. Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in rats indicating that this highly stable PI is capable of surviving passage through the gastrointestinal tract in a biologically active form. Conclusions: To our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestive protease of potential predators, limiting predator's ability to digest egg nutrients. This role has not been reported in the animal kingdom but it is similar to plant defenses against herbivory. Further, this would be the only defense model with no tradeoffs between conspicuousness and noxiousness by encoding into the same molecule both the aposematic warning signal and an antinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probably unpalatable factors would explain the near absence of predators, opening new perspectives in the study of the evolution and ecology of egg defensive strategies.Facultad de Ciencias Naturales y Museo2010info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionArticulohttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://sedici.unlp.edu.ar/handle/10915/29607enginfo:eu-repo/semantics/altIdentifier/url/http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0015059info:eu-repo/semantics/altIdentifier/issn/1932-6203info:eu-repo/semantics/altIdentifier/pmid/21151935info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0015059info:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/2.5/ar/Creative Commons Attribution 2.5 Argentina (CC BY 2.5)reponame:SEDICI (UNLP)instname:Universidad Nacional de La Platainstacron:UNLP2025-09-03T10:29:55Zoai:sedici.unlp.edu.ar:10915/29607Institucionalhttp://sedici.unlp.edu.ar/Universidad públicaNo correspondehttp://sedici.unlp.edu.ar/oai/snrdalira@sedici.unlp.edu.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:13292025-09-03 10:29:55.81SEDICI (UNLP) - Universidad Nacional de La Platafalse
dc.title.none.fl_str_mv The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
title The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
spellingShingle The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
Dreon, Marcos Sebastián
Ciencias Naturales
Bioquímica
Caracoles
predadores
Inhibidores de Serina Proteinasa
embriones
nutrientes
title_short The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
title_full The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
title_fullStr The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
title_full_unstemmed The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
title_sort The role of the proteinase inhibitor ovorubin in apple snail eggs resembles plant embryo defense against predation
dc.creator.none.fl_str_mv Dreon, Marcos Sebastián
Ituarte, Santiago
Heras, Horacio
author Dreon, Marcos Sebastián
author_facet Dreon, Marcos Sebastián
Ituarte, Santiago
Heras, Horacio
author_role author
author2 Ituarte, Santiago
Heras, Horacio
author2_role author
author
dc.subject.none.fl_str_mv Ciencias Naturales
Bioquímica
Caracoles
predadores
Inhibidores de Serina Proteinasa
embriones
nutrientes
topic Ciencias Naturales
Bioquímica
Caracoles
predadores
Inhibidores de Serina Proteinasa
embriones
nutrientes
dc.description.none.fl_txt_mv Background: Fieldwork has thoroughly established that most eggs are intensely predated. Among the few exceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which have virtually no predators. Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuous reddish coloration. The nature of the defense however, was not clear, except for a screening for defenses that identified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinase inhibitor (PI) whose role to protect against pathogens was taken for granted, according to the prevailing assumption. Through biochemical, biophysical and feeding experiments we studied the proteinase inhibitor function of ovorubin in egg defenses. Methodology/Principal Findings: Mass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinase inhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering (SAXS) and crosslinking studies but, in contrast to the classical assumption, it does not prevent bacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis. Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in rats indicating that this highly stable PI is capable of surviving passage through the gastrointestinal tract in a biologically active form. Conclusions: To our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestive protease of potential predators, limiting predator's ability to digest egg nutrients. This role has not been reported in the animal kingdom but it is similar to plant defenses against herbivory. Further, this would be the only defense model with no tradeoffs between conspicuousness and noxiousness by encoding into the same molecule both the aposematic warning signal and an antinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probably unpalatable factors would explain the near absence of predators, opening new perspectives in the study of the evolution and ecology of egg defensive strategies.
Facultad de Ciencias Naturales y Museo
description Background: Fieldwork has thoroughly established that most eggs are intensely predated. Among the few exceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which have virtually no predators. Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuous reddish coloration. The nature of the defense however, was not clear, except for a screening for defenses that identified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinase inhibitor (PI) whose role to protect against pathogens was taken for granted, according to the prevailing assumption. Through biochemical, biophysical and feeding experiments we studied the proteinase inhibitor function of ovorubin in egg defenses. Methodology/Principal Findings: Mass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinase inhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering (SAXS) and crosslinking studies but, in contrast to the classical assumption, it does not prevent bacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis. Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in rats indicating that this highly stable PI is capable of surviving passage through the gastrointestinal tract in a biologically active form. Conclusions: To our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestive protease of potential predators, limiting predator's ability to digest egg nutrients. This role has not been reported in the animal kingdom but it is similar to plant defenses against herbivory. Further, this would be the only defense model with no tradeoffs between conspicuousness and noxiousness by encoding into the same molecule both the aposematic warning signal and an antinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probably unpalatable factors would explain the near absence of predators, opening new perspectives in the study of the evolution and ecology of egg defensive strategies.
publishDate 2010
dc.date.none.fl_str_mv 2010
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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status_str publishedVersion
dc.identifier.none.fl_str_mv http://sedici.unlp.edu.ar/handle/10915/29607
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info:eu-repo/semantics/altIdentifier/pmid/21151935
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0015059
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Creative Commons Attribution 2.5 Argentina (CC BY 2.5)
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Creative Commons Attribution 2.5 Argentina (CC BY 2.5)
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