Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l.

Madeleine Ernst*, Louis Félix Nothias, Justin J.J. van der Hooft, Ricardo R. Silva, C. Haris Saslis-Lagoudakis, Olwen M. Grace, Karen Martinez-Swatson, Gustavo Hassemer, Luís A. Funez, Henrik T. Simonsen, Marnix H. Medema, Dan Staerk, Niclas Nilsson, Paola Lovato, Pieter C. Dorrestein, Nina Rønsted

*Corresponding author for this work

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Abstract

Coevolutionary theory suggests that an arms race between plants and herbivores yields increased plant specialized metabolite diversity and the geographic mosaic theory of coevolution predicts that coevolutionary interactions vary across geographic scales. Consequently, plant specialized metabolite diversity is expected to be highest in coevolutionary hotspots, geographic regions, which exhibit strong reciprocal selection on the interacting species. Despite being well-established theoretical frameworks, technical limitations have precluded rigorous hypothesis testing. Here we aim at understanding how geographic separation over evolutionary time may have impacted chemical differentiation in the cosmopolitan plant genus Euphorbia. We use a combination of state-of-the-art computational mass spectral metabolomics tools together with cell-based high-throughput immunomodulatory testing. Our results show significant differences in specialized metabolite diversity across geographically separated phylogenetic clades. Chemical structural diversity of the highly toxic Euphorbia diterpenoids is significantly reduced in species native to the Americas, compared to Afro-Eurasia. The localization of these compounds to young stems and roots suggest a possible ecological relevance in herbivory defense. This is further supported by reduced immunomodulatory activity in the American subclade as well as herbivore distribution patterns. We conclude that computational mass spectrometric metabolomics coupled with relevant ecological data provide a strong tool for exploring plant specialized metabolite diversity in a chemo-evolutionary framework.

Original languageEnglish
Article number846
JournalFrontiers in Plant Science
Volume10
Number of pages15
ISSN1664-462X
DOIs
Publication statusPublished - 2019

Keywords

  • Coevolution
  • Computational metabolomics
  • Euphorbia
  • Immunomodulatory testing
  • Specialized metabolites

Cite this

Ernst, M., Nothias, L. F., van der Hooft, J. J. J., Silva, R. R., Saslis-Lagoudakis, C. H., Grace, O. M., ... Rønsted, N. (2019). Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l. Frontiers in Plant Science, 10, [846]. https://doi.org/10.3389/fpls.2019.00846
Ernst, Madeleine ; Nothias, Louis Félix ; van der Hooft, Justin J.J. ; Silva, Ricardo R. ; Saslis-Lagoudakis, C. Haris ; Grace, Olwen M. ; Martinez-Swatson, Karen ; Hassemer, Gustavo ; Funez, Luís A. ; Simonsen, Henrik T. ; Medema, Marnix H. ; Staerk, Dan ; Nilsson, Niclas ; Lovato, Paola ; Dorrestein, Pieter C. ; Rønsted, Nina. / Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l. In: Frontiers in Plant Science. 2019 ; Vol. 10.
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title = "Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l.",
abstract = "Coevolutionary theory suggests that an arms race between plants and herbivores yields increased plant specialized metabolite diversity and the geographic mosaic theory of coevolution predicts that coevolutionary interactions vary across geographic scales. Consequently, plant specialized metabolite diversity is expected to be highest in coevolutionary hotspots, geographic regions, which exhibit strong reciprocal selection on the interacting species. Despite being well-established theoretical frameworks, technical limitations have precluded rigorous hypothesis testing. Here we aim at understanding how geographic separation over evolutionary time may have impacted chemical differentiation in the cosmopolitan plant genus Euphorbia. We use a combination of state-of-the-art computational mass spectral metabolomics tools together with cell-based high-throughput immunomodulatory testing. Our results show significant differences in specialized metabolite diversity across geographically separated phylogenetic clades. Chemical structural diversity of the highly toxic Euphorbia diterpenoids is significantly reduced in species native to the Americas, compared to Afro-Eurasia. The localization of these compounds to young stems and roots suggest a possible ecological relevance in herbivory defense. This is further supported by reduced immunomodulatory activity in the American subclade as well as herbivore distribution patterns. We conclude that computational mass spectrometric metabolomics coupled with relevant ecological data provide a strong tool for exploring plant specialized metabolite diversity in a chemo-evolutionary framework.",
keywords = "Coevolution, Computational metabolomics, Euphorbia, Immunomodulatory testing, Specialized metabolites",
author = "Madeleine Ernst and Nothias, {Louis F{\'e}lix} and {van der Hooft}, {Justin J.J.} and Silva, {Ricardo R.} and Saslis-Lagoudakis, {C. Haris} and Grace, {Olwen M.} and Karen Martinez-Swatson and Gustavo Hassemer and Funez, {Lu{\'i}s A.} and Simonsen, {Henrik T.} and Medema, {Marnix H.} and Dan Staerk and Niclas Nilsson and Paola Lovato and Dorrestein, {Pieter C.} and Nina R{\o}nsted",
year = "2019",
doi = "10.3389/fpls.2019.00846",
language = "English",
volume = "10",
journal = "Frontiers in Plant Science",
issn = "1664-462X",
publisher = "Frontiers Media S.A.",

}

Ernst, M, Nothias, LF, van der Hooft, JJJ, Silva, RR, Saslis-Lagoudakis, CH, Grace, OM, Martinez-Swatson, K, Hassemer, G, Funez, LA, Simonsen, HT, Medema, MH, Staerk, D, Nilsson, N, Lovato, P, Dorrestein, PC & Rønsted, N 2019, 'Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l.', Frontiers in Plant Science, vol. 10, 846. https://doi.org/10.3389/fpls.2019.00846

Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l. / Ernst, Madeleine; Nothias, Louis Félix; van der Hooft, Justin J.J.; Silva, Ricardo R.; Saslis-Lagoudakis, C. Haris; Grace, Olwen M.; Martinez-Swatson, Karen; Hassemer, Gustavo; Funez, Luís A.; Simonsen, Henrik T.; Medema, Marnix H.; Staerk, Dan; Nilsson, Niclas; Lovato, Paola; Dorrestein, Pieter C.; Rønsted, Nina.

In: Frontiers in Plant Science, Vol. 10, 846, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l.

AU - Ernst, Madeleine

AU - Nothias, Louis Félix

AU - van der Hooft, Justin J.J.

AU - Silva, Ricardo R.

AU - Saslis-Lagoudakis, C. Haris

AU - Grace, Olwen M.

AU - Martinez-Swatson, Karen

AU - Hassemer, Gustavo

AU - Funez, Luís A.

AU - Simonsen, Henrik T.

AU - Medema, Marnix H.

AU - Staerk, Dan

AU - Nilsson, Niclas

AU - Lovato, Paola

AU - Dorrestein, Pieter C.

AU - Rønsted, Nina

PY - 2019

Y1 - 2019

N2 - Coevolutionary theory suggests that an arms race between plants and herbivores yields increased plant specialized metabolite diversity and the geographic mosaic theory of coevolution predicts that coevolutionary interactions vary across geographic scales. Consequently, plant specialized metabolite diversity is expected to be highest in coevolutionary hotspots, geographic regions, which exhibit strong reciprocal selection on the interacting species. Despite being well-established theoretical frameworks, technical limitations have precluded rigorous hypothesis testing. Here we aim at understanding how geographic separation over evolutionary time may have impacted chemical differentiation in the cosmopolitan plant genus Euphorbia. We use a combination of state-of-the-art computational mass spectral metabolomics tools together with cell-based high-throughput immunomodulatory testing. Our results show significant differences in specialized metabolite diversity across geographically separated phylogenetic clades. Chemical structural diversity of the highly toxic Euphorbia diterpenoids is significantly reduced in species native to the Americas, compared to Afro-Eurasia. The localization of these compounds to young stems and roots suggest a possible ecological relevance in herbivory defense. This is further supported by reduced immunomodulatory activity in the American subclade as well as herbivore distribution patterns. We conclude that computational mass spectrometric metabolomics coupled with relevant ecological data provide a strong tool for exploring plant specialized metabolite diversity in a chemo-evolutionary framework.

AB - Coevolutionary theory suggests that an arms race between plants and herbivores yields increased plant specialized metabolite diversity and the geographic mosaic theory of coevolution predicts that coevolutionary interactions vary across geographic scales. Consequently, plant specialized metabolite diversity is expected to be highest in coevolutionary hotspots, geographic regions, which exhibit strong reciprocal selection on the interacting species. Despite being well-established theoretical frameworks, technical limitations have precluded rigorous hypothesis testing. Here we aim at understanding how geographic separation over evolutionary time may have impacted chemical differentiation in the cosmopolitan plant genus Euphorbia. We use a combination of state-of-the-art computational mass spectral metabolomics tools together with cell-based high-throughput immunomodulatory testing. Our results show significant differences in specialized metabolite diversity across geographically separated phylogenetic clades. Chemical structural diversity of the highly toxic Euphorbia diterpenoids is significantly reduced in species native to the Americas, compared to Afro-Eurasia. The localization of these compounds to young stems and roots suggest a possible ecological relevance in herbivory defense. This is further supported by reduced immunomodulatory activity in the American subclade as well as herbivore distribution patterns. We conclude that computational mass spectrometric metabolomics coupled with relevant ecological data provide a strong tool for exploring plant specialized metabolite diversity in a chemo-evolutionary framework.

KW - Coevolution

KW - Computational metabolomics

KW - Euphorbia

KW - Immunomodulatory testing

KW - Specialized metabolites

U2 - 10.3389/fpls.2019.00846

DO - 10.3389/fpls.2019.00846

M3 - Journal article

VL - 10

JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

SN - 1664-462X

M1 - 846

ER -

Ernst M, Nothias LF, van der Hooft JJJ, Silva RR, Saslis-Lagoudakis CH, Grace OM et al. Assessing specialized metabolite diversity in the cosmopolitan plant genus Euphorbia l. Frontiers in Plant Science. 2019;10. 846. https://doi.org/10.3389/fpls.2019.00846