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

Madeleine Ernst; Louis-Félix Nothias; Justin van der Hooft; Ricardo R. da Silva; Haris Saslis Lagoudakis; Olwen M Grace; Karen Agatha Martinez-Swatson; Gustavo Hassemer; Luis A. Funez; Henrik Toft Simonsen; Marnix H. Medema; Dan Stærk; Niclas Nilsson; Paola Lovato; Pieter C. Dorrestein; Nina Rønsted

doi:10.3389/fpls.2019.00846

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

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

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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 language	English
Article number	846
Journal	Frontiers in Plant Science
Volume	10
ISSN	1664-462X
DOIs	https://doi.org/10.3389/fpls.2019.00846
Publication status	Published - 31 May 2019

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Ernst, M., Nothias, L-F., van der Hooft, J., da Silva, R. R., Saslis Lagoudakis, H., Grace, O. M., Martinez-Swatson, K. A., Hassemer, G., Funez, L. A., Simonsen, H. T., Medema, M. H., Stærk, D., Nilsson, N., Lovato, P., Dorrestein, P. C., & 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, M, Nothias, L-F, van der Hooft, J, da Silva, RR, Saslis Lagoudakis, H, Grace, OM, Martinez-Swatson, KA, Hassemer, G, Funez, LA, Simonsen, HT, Medema, MH, Stærk, 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

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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.",

author = "Madeleine Ernst and Louis-F{\'e}lix Nothias and {van der Hooft}, Justin and {da Silva}, {Ricardo R.} and {Saslis Lagoudakis}, Haris and Grace, {Olwen M} and Martinez-Swatson, {Karen Agatha} and Gustavo Hassemer and Funez, {Luis A.} and Simonsen, {Henrik Toft} and Medema, {Marnix H.} and Dan St{\ae}rk and Niclas Nilsson and Paola Lovato and Dorrestein, {Pieter C.} and Nina R{\o}nsted",

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doi = "10.3389/fpls.2019.00846",

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AU - Ernst, Madeleine

AU - Nothias, Louis-Félix

AU - van der Hooft, Justin

AU - da Silva, Ricardo R.

AU - Saslis Lagoudakis, Haris

AU - Grace, Olwen M

AU - Martinez-Swatson, Karen Agatha

AU - Hassemer, Gustavo

AU - Funez, Luis A.

AU - Simonsen, Henrik Toft

AU - Medema, Marnix H.

AU - Stærk, Dan

AU - Nilsson, Niclas

AU - Lovato, Paola

AU - Dorrestein, Pieter C.

AU - Rønsted, Nina

PY - 2019/5/31

Y1 - 2019/5/31

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.

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DO - 10.3389/fpls.2019.00846

M3 - Journal article

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SN - 1664-462X

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JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

M1 - 846

ER -

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

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