Assessing Specialized Metabolite Diversity in the Cosmopolitan Plant Genus Euphorbia L.

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

doi:10.3389/fpls.2019.00846

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.

Highlights

As a consequence of niche colonization and adaptive evolution, plants produce an extraordinary variety of molecules
Chamaesyce and previous observations of Euphorbia diterpenoids exhibiting anti-herbivore biological activity (Batra, 1983; Hundsdoerfer et al, 2005a; Huang et al, 2014; Hua et al, 2017), we find very few to no Euphorbia diterpenoids in representatives of the American radiation of subg
We hypothesized that specialized metabolite diversity would show significant phylogenetic structure in Euphorbia, which could be driven by the chemical structural diversity of metabolites potentially used in the defense against herbivory

Summary

Introduction

As a consequence of niche colonization and adaptive evolution, plants produce an extraordinary variety of molecules These so-called specialized metabolites are deployed in the response to a multitude of biotic as well as abiotic factors (Bednarek and Osbourn, 2009), for example, to attract pollinators or seed-dispersing animals, in signaling between other plants and symbiotic microorganisms or to combat herbivores or physical stresses such as UV light (Bednarek and Osbourn, 2009; Wink, 2010). Detoxification profiles of the parsnip webworm Depressaria pastinacella (Duponchel, 1838) and plant defense profiles of its host, the wild parsnip (Pastinaca sativa L.) were significantly mismatched in the presence of an alternate host plant, the cow parsnip (Heracleum lanatum Michx.) This suggests that the presence of a chemically different alternate host can affect selection intensity and patterns of reciprocal response across landscapes (Zangerl and Berenbaum, 2003). In widespread species, an inevitable consequence of the geographic mosaic of coevolution is the formation of highly divergent populations that have the potential to form new species (Thompson, 2008)

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Conclusion