© 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.  The attached file is the published version of the article

Altschul

Benson

Berch

Berner

Bidartondo

Cameron

Carafa

Crandall-Stotler

Dalpe

David J. Beerling

Desiró

Duckett

Duncan D. Cameron

Edgar

Field

Fletcher

Gardes

Heinrichs

Huelsenbeck

Humphreys

James

Javot

Jeffrey G. Duckett

Johnson

Jonathan R. Leake

Kate E. Allinson

Katie J. Field

Kiers

Klekowski

Ligrone

Malloch

Martin I. Bidartondo

Nobel

Olsson

Parniske

Parry

Pirozynski

Pressel

Read

Redecker

Remy

Schloss

Selosse

Silvia Pressel

Simon

Smit

Smith

Strullu-Derrien

Stubblefield

Tamura

Taylor

Tisserant

Wang

White

William R. Rimington

New Phytologist

© 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.  The attached file is the published version of the article.NHM Repositor

Field, KJ

Rimington, WR

Bidartondo, MI

Allinson, KE

Beerling, DJ

Cameron, DD

Duckett, JG

Leake, JR

Pressel, S

Natural History Museum Repository

English

1993.Occurrence of non-mycorrhizal plant species in south Swedish rocky habitats is related to exchangeable soil phosphate.

2001.MRBAYES: bayesian inference of phylogenetic trees.

2006.Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens.

2007.Mycorrhizal acquisition of inorganic phosphorus by the green-leaved terrestrial orchid Goodyera repens.

2010.Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants.

205: 743–756 www.newphytologist.com

A high-precision U-Pb age constraint on the Rhynie Chert Konservat-Lagerstatte: time scale and other implications.

A novel ascomycetous endophytic association in the rhizoids of the leafy liverwort family, Schistochilaceae (Jungermanniidae, Hepaticopsida).

Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis.

and diversification of endomycorrhizal fungi and coincidence with vascular land plants.

Arbuscular mycorrhiza: the mother of plant root endosymbioses.

Conflicting phylogenies for early land plants are caused by composition biases among synonymous substitutions.

Conservative ecological and evolutionary patterns in liverwort–fungal symbioses.

Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review).

Endogone pisiformis – axenic culture and associations with Sphagnum, Pinus sylvestris, Allium cepa and Allium porrum.

Endogone pisiformis: growth, morphology, and maintenance of cultures.

Evolution of leafy liverworts (Jungermanniidae, Marchantiophyta): estimating divergence times from chloroplast DNA sequences using penalized likelihood with integrated fossil evidence.

Fossil arbuscular mycorrhizae from the early Devonian.Mycologia

Fossil mycorrhizae – a case for symbiosis.

Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses.

Fungal CO2, O2, light and temperature.

Fungal symbioses in bryophytes: new insights in the twenty-first century.

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.

Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.

GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2.

Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens.

Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis.

Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.

ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts.

Major transitions in the evolution of early land plants: a bryological perspective.

MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Molecular

Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks.

Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles.

Phylogeny and classifications of the Marchantiophyta.

Phylogeny of the Glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers.Mycologia 98:

Physicochemical and environmental plant physiology, 2nd edn. Amsterdam, the Netherlands:

Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants.

Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis.

Reconstructing the early evolution of fungi using a six-gene phylogeny.

Reproductive biology of the Pteridophyta. III. A study of the Blechnaceae.

Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus.

Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi.

symbiosis, 3rd edn.

Symbiotic fungal associations in ‘lower’ land plants.

The Authors New Phytologist

The dawn of symbiosis between plants and fungi.

The land flora: a phototroph–fungus partnership?

The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus.

The origin of land plants: a matter of mycotrophism.

Towards a natural classification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL.

Ultrastructure of a fungal endophyte in Phaeoceros laevis

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO 2

Field, K.J.

Rimington, W.R.

Bidartondo, M.I.

Allinson, K.E.

Beerling, D.J.

Cameron, D.D.

Duckett, J.G.

Leake, J.R.

Pressel, S.

The University of Manchester - Institutional Repository

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO&lt;inf&gt;2&lt;/inf&gt;

Crossref

First evidence of mutualism between ancient plant lineages (
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            aplomitriopsida liverworts) and
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            ucoromycotina fungi and its response to simulated
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            alaeozoic changes in atmospheric
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White Rose Research Online

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2

The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that Glomeromycota formed the sole ancestral plant-fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO2 concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon-for-nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid-Palaeozoic (1500 ppm) and near-contemporary (440 ppm) CO2 concentrations using isotope tracers, and analysed cytological differences in plant-fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort-Mucoromycotina symbiosis is mutualistic and mycorrhiza-like, but differs from liverwort-Glomeromycota symbiosis in maintaining functional efficiency of carbon-for-nutrient exchange between partners across CO2 concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild-collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO2 , we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis

Spiral - Imperial College Digital Repository

https://eprints.whiterose.ac.uk/89234/1/First%20evidence%20of%20mutualism%20between%20ancient%20plant%20lineages%20%28Haplomitriopsida%20liverworts%29%20and%20Mucoromycotina%20fungi%20and%20its%20response%20to%20simulated%20Palaeozoic%20changes%20in%20atmospheric%20CO2..pdf

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2

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Spiral - Imperial College Digital Repository

The University of Manchester - Institutional Repository

White Rose Research Online

White Rose Research Online

White Rose Research Online