Weak population spatial genetic structure and low infraspecific specificity for fungal partners in the rare mycoheterotrophic orchid Epipogium aphyllum

Julita Minasiewicz,Tiiu Kull,Joanna Znaniecka,Lucie Vincenot,Emilia Krawczyk,Marc-André Selosse,Ekaterina Zheleznaya,Joanna Korybut-Orlowska

doi:10.1007/s10265-021-01364-7

Abstract

Some plants abandoned photosynthesis and developed full dependency on fungi for nutrition. Most of the so-called mycoheterotrophic plants exhibit high specificity towards their fungal partners. We tested whether natural rarity of mycoheterotrophic plants and usual small and fluctuating population size make their populations more prone to genetic differentiation caused by restricted gene flow and/or genetic drift. We also tested whether these genetic characteristics might in turn shape divergent fungal preferences. We studied the mycoheterotrophic orchid Epipogium aphyllum, addressing the joint issues of genetic structure of its populations over Europe and possible consequences for mycorrhizal specificity within the associated fungal taxa. Out of 27 sampled E. aphyllum populations, nine were included for genetic diversity assessment using nine nuclear microsatellites and plastid DNA. Population genetic structure was inferred based on the total number of populations. Individuals from 17 locations were included into analysis of genetic identity of mycorrhizal fungi of E. aphyllum based on barcoding by nuclear ribosomal DNA. Epipogium aphyllum populations revealed high genetic diversity (uHe = 0.562) and low genetic differentiation over vast distances (FST = 0.106 for nuclear microsatellites and FST = 0.156 for plastid DNA). Bayesian clustering analyses identified only two genetic clusters, with a high degree of admixture. Epipogium aphyllum genets arise from panmixia and display locally variable, but relatively high production of ramets, as shown by a low value of rarefied genotypic richness (Rr = 0.265). Epipogium aphyllum genotype control over partner selection was negligible as (1) we found ramets from a single genetic individual associated with up to 68% of the known Inocybe spp. associating with the plant species, (2) and partner identity did not show any geographic structure. The absence of mosaicism in the mycorrhizal specificity over Europe may be linked to preferential allogamous habit of E. aphyllum and significant gene flow, which tend to promote host generalism.

Highlights

Mycoheterotrophy, the ability to obtain organic carbon from mycorrhizal fungi, supports the nutrition of some achlorophyllous plants (Leake 1994)
Most mycoheterotrophic plants (MHP) associate with mycorrhizal fungi, which are themselves associated with surrounding autotrophic plants; they cheat on a mycorrhizal network built on an otherwise mutualistic symbiosis, where photosynthates from autotrophic plants are exchanged for water and soil minerals collected by fungal partners (Jacquemyn and Merckx 2019; Selosse and Rousset 2011)
Our study addresses the joint issues of genetic diversity, spatial genetic structure and inferred gene flow in allogamous E. aphyllum over Eurasia with a focus on Europe, and their possible consequences for interaction with its mycorrhizal partners

Summary

Introduction

Mycoheterotrophy, the ability to obtain organic carbon from mycorrhizal fungi, supports the nutrition of some achlorophyllous plants (Leake 1994). Mycoheterotrophic plants common characteristics, such as usual small population size and often fluctuating numbers of individuals (Merckx 2013) as well as frequently observed autogamy (Waterman et al 2013) may entail lower gene flow and genetic drift. This could lead to differentiation of populations and evolution of divergent specialisation towards mycorrhizal fungi through narrowing specialisation for fungal partner, as with the loss of genetic diversity plants may lose the ability to cheat on certain fungi (see Kennedy et al 2011)

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