Macroevolutionary decline in mycorrhizal colonization and chemical defense responsiveness to mycorrhization

Ludovico Formenti; Natalie Iwanycki Ahlstrand; Gustavo Hassemer; Gaëtan Glauser; Johan van den Hoogen; Nina Rønsted; Marcel van der Heijden; Thomas W Crowther; Sergio Rasmann

doi:10.1016/j.isci.2023.106632

Macroevolutionary decline in mycorrhizal colonization and chemical defense responsiveness to mycorrhization

iScience. 2023 Apr 10;26(5):106632. doi: 10.1016/j.isci.2023.106632. eCollection 2023 May 19.

Authors

Affiliations

¹ Laboratory of Functional Ecology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
² Institute of Ecology and Evolution, Terrestrial ecology, University of Bern, Bern, Switzerland.
³ Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
⁴ Neuchâtel Platform of Analytical Chemistry (NPAC), University of Neuchâtel, Neuchâtel, Switzerland.
⁵ Department of Environmental Systems Science, Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland.
⁶ National Tropical Botanical Garden, Kalaheo, HI 96741, USA.
⁷ Plant-Soil Interactions, Institute for Sustainability Sciences, Agroscope, 8046 Zürich, Switzerland.

Abstract

Arbuscular mycorrhizal fungi (AMF) have evolved associations with roots of 60% plant species, but the net benefit for plants vary broadly from mutualism to parasitism. Yet, we lack a general understanding of the evolutionary and ecological forces driving such variation. To this end, we conducted a comparative phylogenetic experiment with 24 species of Plantago, encompassing worldwide distribution, to address the effect of evolutionary history and environment on plant growth and chemical defenses in response to AMF colonization. We demonstrate that different species within one plant genus vary greatly in their ability to associate with AMF, and that AMF arbuscule colonization intensity decreases monotonically with increasing phylogenetic branch length, but not with concomitant changes in pedological and climatic conditions across species. Moreover, we demonstrate that species with the highest colonization levels are also those that change their defensive chemistry the least. We propose that the costs imposed by high AMF colonization in terms of reduced changes in secondary chemistry might drive the observed macroevolutionary decline in mycorrhization.

Keywords: Microbiome; Plant ecology; Plant evolution.