Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)

Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of...

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Auteur principal: Coley, Phyllis (author)
Autres auteurs: Endara, María-José (author), Ghabash, Gabrielle (author), Kinder, Catherine (author), Nicholls, James (author), Pennington, R. Toby (author), Mills, Anthony (author), Soule, Abrianna (author), Lemes, Maristerra (author), Stone, Graham (author), Kursar, Thomas (author)
Format: article
Langue:eng
Publié: 2019
Accès en ligne:https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13208
https://hdl.handle.net/20.500.14809/3071
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author Coley, Phyllis
author2 Endara, María-José
Ghabash, Gabrielle
Kinder, Catherine
Nicholls, James
Pennington, R. Toby
Mills, Anthony
Soule, Abrianna
Lemes, Maristerra
Stone, Graham
Kursar, Thomas
author2_role author
author
author
author
author
author
author
author
author
author
author_facet Coley, Phyllis
Endara, María-José
Ghabash, Gabrielle
Kinder, Catherine
Nicholls, James
Pennington, R. Toby
Mills, Anthony
Soule, Abrianna
Lemes, Maristerra
Stone, Graham
Kursar, Thomas
author_role author
collection Repositorio Universidad Tecnológica Indoamérica
dc.creator.none.fl_str_mv Coley, Phyllis
Endara, María-José
Ghabash, Gabrielle
Kinder, Catherine
Nicholls, James
Pennington, R. Toby
Mills, Anthony
Soule, Abrianna
Lemes, Maristerra
Stone, Graham
Kursar, Thomas
dc.date.none.fl_str_mv 2019
2022-06-13T00:25:44Z
2022-06-13T00:25:44Z
dc.identifier.none.fl_str_mv https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13208
https://hdl.handle.net/20.500.14809/3071
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Journal of Ecology. Volume 107, Issue 4, Pages 1620 - 1632
dc.rights.none.fl_str_mv https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
dc.source.none.fl_str_mv reponame:Repositorio Universidad Tecnológica Indoamérica
instname:Universidad Tecnológica Indoamérica
instacron:UTI
dc.title.none.fl_str_mv Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
dc.type.none.fl_str_mv info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/article
description Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L-tyrosine and its role as a defence against herbivores. We examined overexpression of tyrosine in 97 species of Inga (Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti-herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations. Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L-tyrosine, Inga species with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine-producing species also contained secondary metabolites that are derived from tyrosine: tyrosine-gallates, tyramine-gallates and DOPA-gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants. Synthesis. We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti-herbivore defences.
eu_rights_str_mv openAccess
format article
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instname_str Universidad Tecnológica Indoamérica
language eng
network_acronym_str UTI
network_name_str Repositorio Universidad Tecnológica Indoamérica
oai_identifier_str oai:repositorio.uti.edu.ec:20.500.14809/3071
publishDate 2019
publisher.none.fl_str_mv Journal of Ecology. Volume 107, Issue 4, Pages 1620 - 1632
reponame_str Repositorio Universidad Tecnológica Indoamérica
repository.mail.fl_str_mv .
repository.name.fl_str_mv Repositorio Universidad Tecnológica Indoamérica - Universidad Tecnológica Indoamérica
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rights_invalid_str_mv https://creativecommons.org/licenses/by/4.0/
spelling Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)Coley, PhyllisEndara, María-JoséGhabash, GabrielleKinder, CatherineNicholls, JamesPennington, R. TobyMills, AnthonySoule, AbriannaLemes, MaristerraStone, GrahamKursar, ThomasPlant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L-tyrosine and its role as a defence against herbivores. We examined overexpression of tyrosine in 97 species of Inga (Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti-herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations. Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L-tyrosine, Inga species with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine-producing species also contained secondary metabolites that are derived from tyrosine: tyrosine-gallates, tyramine-gallates and DOPA-gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants. Synthesis. We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti-herbivore defences.Journal of Ecology. Volume 107, Issue 4, Pages 1620 - 16322022-06-13T00:25:44Z2022-06-13T00:25:44Z2019info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13208https://hdl.handle.net/20.500.14809/3071enghttps://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessreponame:Repositorio Universidad Tecnológica Indoaméricainstname:Universidad Tecnológica Indoaméricainstacron:UTI2022-06-18T23:29:57Zoai:repositorio.uti.edu.ec:20.500.14809/3071Institucionalhttps://repositorio.uti.edu.ec/Institución privadahttps://indoamerica.edu.ec/https://repositorio.uti.edu.ec/oai.Ecuador...opendoar:02022-06-18T23:29:57Repositorio Universidad Tecnológica Indoamérica - Universidad Tecnológica Indoaméricafalse
spellingShingle Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
Coley, Phyllis
status_str publishedVersion
title Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
title_full Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
title_fullStr Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
title_full_unstemmed Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
title_short Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
title_sort Macroevolutionary patterns in overexpression of tyrosine: An anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)
url https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.13208
https://hdl.handle.net/20.500.14809/3071