Symbiont switching and trophic mode shifts in Orchidaceae.

Deyi Wang,Vincent S F T Merckx,Rutger A Vos,Sofia I F Gomes,Hans Jacquemyn

doi:10.1111/nph.17414

Deyi Wang, Vincent S F T Merckx + Show 3 more

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https://doi.org/10.1111/nph.17414

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Abstract

Summary Mycorrhizal fungi are central to the biology of land plants. However, to what extent mycorrhizal shifts – broad evolutionary transitions in root‐associated fungal symbionts – are related to changes in plant trophic modes remains poorly understood.We built a comprehensive DNA dataset of Orchidaceae fungal symbionts and a dated plant molecular phylogeny to test the hypothesis that shifts in orchid trophic modes follow a stepwise pattern, from autotrophy over partial mycoheterotrophy (mixotrophy) to full mycoheterotrophy, and that these shifts are accompanied by switches in fungal symbionts.We estimate that at least 17 independent shifts from autotrophy towards full mycoheterotrophy occurred in orchids, mostly through an intermediate state of partial mycoheterotrophy. A wide range of fungal partners was inferred to occur in the roots of the common ancestor of this family, including ‘rhizoctonias’, ectomycorrhizal, and wood‐ or litter‐decaying saprotrophic fungi. Phylogenetic hypothesis tests further show that associations with ectomycorrhizal or saprotrophic fungi were most likely a prerequisite for evolutionary shifts towards full mycoheterotrophy.We show that shifts in trophic mode often coincided with switches in fungal symbionts, suggesting that the loss of photosynthesis selects for different fungal communities in orchids. We conclude that changes in symbiotic associations and ecophysiological traits are tightly correlated throughout the diversification of orchids.

Highlights

The history of evolution and biodiversity is fundamentally a history of the evolution of species interactions (Margulis, 1991; Thompson, 1999, 2005)
After removing fungal families that associated with a single orchid species, a total of 68 fungal families in Basidiomycota and Ascomycota were identified based on internal transcribed spacer (ITS) sequences generated from both Sanger and high-throughput sequencing (HTS) techniques (Fig. S1)
Seventeen of all detected fungal families that have previously been identified as putative orchid mycorrhiza fungi (Dearnaley et al, 2012) were mapped on the orchid phylogeny (Figs 1, S4), including three rhizoctonia families (Tulasnellaceae, Ceratobasidiaceae and Serendipitaceae), seven families mainly comprising ECM fungi (Sebacinaceae, Thelephoraceae, Russulaceae, Tuberaceae, Clavulinaceae, Hymenogastraceae, Inocybaceae), and seven families containing SAP and/or ECM fungi (Pezizaceae, Pyronemataceae, Hymenochaetaceae, Marasmiaceae, Psathyrellaceae, Mycenaceae, Physalacriaceae)

Summary

Introduction

The history of evolution and biodiversity is fundamentally a history of the evolution of species interactions (Margulis, 1991; Thompson, 1999, 2005). Recent studies have suggested that the composition of mycorrhizal fungal communities differs between plant nutritional modes, ranging from an exclusively autotrophic to a fully mycoheterotrophic mode of life, in which photosynthesis has been replaced by the uptake of carbon from root-associated fungi (Yagame et al, 2016; Jacquemyn & Merckx, 2019). This raises the hypothesis that shifts in trophic modes are correlated with switches in symbiotic associations in land plants

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