Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline.

Katie J Field,Silvia Pressel,Jonathan R Leake,Kate E Allinson,David J Beerling,Duncan D Cameron,William R Rimington,Jeffrey G Duckett,Martin I Bidartondo

doi:10.1038/ismej.2015.204

Abstract

Most land plants form mutualistic associations with arbuscular mycorrhizal fungi of the Glomeromycota, but recent studies have found that ancient plant lineages form mutualisms with Mucoromycotina fungi. Simultaneous associations with both fungal lineages have now been found in some plants, necessitating studies to understand the functional and evolutionary significance of these tripartite associations for the first time. We investigate the physiology and cytology of dual fungal symbioses in the early-diverging liverworts Allisonia and Neohodgsonia at modern and Palaeozoic-like elevated atmospheric CO2 concentrations under which they are thought to have evolved. We found enhanced carbon cost to liverworts with simultaneous Mucoromycotina and Glomeromycota associations, greater nutrient gain compared with those symbiotic with only one fungal group in previous experiments and contrasting responses to atmospheric CO2 among liverwort–fungal symbioses. In liverwort–Mucoromycotina symbioses, there is increased P-for-C and N-for-C exchange efficiency at 440 p.p.m. compared with 1500 p.p.m. CO2. In liverwort–Glomeromycota symbioses, P-for-C exchange is lower at ambient CO2 compared with elevated CO2. No characteristic cytologies of dual symbiosis were identified. We provide evidence of a distinct physiological niche for plant symbioses with Mucoromycotina fungi, giving novel insight into why dual symbioses with Mucoromycotina and Glomeromycota fungi persist to the present day.

Highlights

Symbioses with soil fungi have existed since plants first began to colonize the Earth’s land masses (Redecker et al, 2000; Redecker and Raab, 2006; Smith and Read, 2008) and are thought to have played a key role in establishing terrestrial ecosystems (Pirozynski and Malloch, 1975; Malloch et al, 1980)
(2) Do plants with dual colonization by Mucoro-We investigated the functionality and detailed mycotina and Glomeromycota fungi benefit cytology of the dual fungal associations in wildfrom enhanced nutrient gain in comparison to collected Neohodgsonia mirabilis, the sister taxon to those harbouring single fungal associations?
2008, 2009; Villarreal et al, 2015) (Figure 1). (4) Are there any characteristic cytological signa-. We found that both tures of dual fungal symbiosis as opposed to liverworts hosted simultaneous Glomeromycota single fungal associations?

Summary

Introduction

Symbioses with soil fungi have existed since plants first began to colonize the Earth’s land masses (Redecker et al, 2000; Redecker and Raab, 2006; Smith and Read, 2008) and are thought to have played a key role in establishing terrestrial ecosystems (Pirozynski and Malloch, 1975; Malloch et al, 1980). We can begin insoluble starch granules within the thallus to answer this question with the present demonstration (observed here in Allisonia; Figure 6h), supplied that dual associations are significantly more efficient at directly to fungal partner(s) (see Figures 3a and b), or modern day atmospheric CO2 compared with Palaeo- be released into the surrounding soil as exudates.

Objectives

Results

Conclusion