Short Title: Vascular plant-Mucoromycotina fungal symbiosis · 65 Glomeromycotina fungi in the same plant host (Desirò et al., 2013; Rimington et al., 2015). 66 Mucoromycotina represents
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1
Short Title: Vascular plant-Mucoromycotina fungal symbiosis 1
2
* Corresponding author: Katie J. Field ([email protected]); Tel: +44 (0)113 343 2849 3
4
Mucoromycotina fine root endophyte fungi form nutritional mutualisms with vascular 5
plants 6
7
Grace A. Hoysted1, Alison S. Jacob2,3, Jill Kowal4, Philipp Giesemann5, Martin I. Bidartondo2,3, 8
Jeffrey G. Duckett4, Gerhard Gebauer5, William R. Rimington2,3,4, Sebastian Schornack6, Silvia 9
Pressel4, and Katie J. Field1* 10
11
1 Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, LS2 12
Holcus* S root intracellular and intercellular, small ICSs
coarse hyphae (>3 µm), large vesicles (20-40 µm), fine hyphae (0.5-1.5 µm) with small vesicles (5-10 µm), arbuscules/arbuscule-like structures
(M&G)*
Molinia* S root intracellular and intercellular, small ICSs
coarse hyphae (>3 µm), large vesicles (20-40 µm), fine hyphae (0.5-1.5 µm) with small vesicles/swellings (5-10 µm), arbuscules/arbuscule-like structures
(M&G)*
Juncus* S root intracellular and intercellular, small ICSs
coarse hyphae (>3 µm), large vesicles (20-40 µm), fine hyphae (0.5-1.5 µm) with small vesicles (5-10 µm), arbuscules/arbuscule-like structures
(M&G)*
Trifolium1 S root intracellular and intercellular, small ICSs
coarse hyphae (>3 m),
large vesicles (>30 m)
fine hyphae (>1.5 m), intercalary and terminal vesicles/swellings (5-10
m) and arbuscules/arbuscule-like structures
(M&G)1 Orchard et al. 2017a
Fossils
Horneophyton1 S aerial axes, cortical cells
intracellular coarse hyphae (>3 m), large vesicles (up to 50
m), arbuscule-like structures
G1 Strullu-Derrien et al. 2014
corm intracellular and intercellular
intracellular coils, intercellular coarse
hyphae (11-13 m), thick-walled fungal structures
M1
Nothia1 S aerial and prostrate axes
Intercellular and intracellular
coarse hyphae (up to 15
m) and intercellular
vesicles (>50 m)
? Krings et al. 2007
598
Figure legends 599
Figure 1. Land plant phylogeny and species used in the present study. (a) Land plant 600
Albornoz FE, Lambers H, Turner BL, Teste FP, Laliberté E (2016) Shifts in symbiotic 653
associations in plants capable of forming multiple root symbioses across a long‐654
term soil chronosequence. Ecology and Evolution 6: 2368-2377 655 Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular 656
in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between 659 forest orchids and trees. Proceedings of the Royal Society of London B: Biological 660 Sciences 271: 1799-1806 661
Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn 662 of symbiosis between plants and fungi. Biology Letters: rsbl20101203 663
Brundrett M, Bougher N, Dell B, Grove T (1996) Working with Mycorrhizas in Forestry and 664 Agriculture. 665
Cameron DD, Johnson I, Leake JR, Read DJ (2007) Mycorrhizal acquisition of inorganic 666 phosphorus by the green-leaved terrestrial orchid Goodyera repens. Annals of 667 Botany 99: 831-834 668
Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycorrhiza in orchids: evidence from 669
plant–fungus carbon and nitrogen transfers in the green‐leaved terrestrial orchid 670
Goodyera repens. New Phytologist 171: 405-416 671 Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, 672
Williams DG, Reich PB, Ellsworth DS (2009) Why are non-photosynthetic tissues 673 generally 13C enriched compared with leaves in C3 plants? Review and synthesis of 674 current hypotheses. Functional Plant Biology 36: 199-213 675
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in 676 plant ecology. Annual Review of Ecology and Systematics 33: 507-559 677
Desirò A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses 678 in hornworts: a chequered history. Proceedings of the Royal Society of London B: 679 Biological Sciences 280: 20130207 680
Duckett JG, Carafa A, Ligrone R (2006) A highly differentiated glomeromycotean 681 association with the mucilage-secreting, primitive antipodean liverwort Treubia 682 (Treubiaceae): clues to the origins of mycorrhizas. American Journal of Botany 93: 683 797-813 684
Duckett JG, Ligrone R (1992) A light and electron microscope study of the fungal 685 endophytes in the sporophyte and gametophyte of Lycopodium cernuum with 686 observations on the gametophyte–sporophyte junction. Canadian Journal of Botany 687 70: 58-72 688
Edgar R (2016) UCHIME2: improved chimera prediction for amplicon sequencing. bioRxiv: 689 074252 690
Farquhar GD, O'Leary MH, Berry JA (1982) On the relationship between carbon isotope 693 discrimination and the intercellular carbon dioxide concentration in leaves. Functional 694 Plant Biology 9: 121-137 695
Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling DJ, Cameron DD, 696 Duckett JG, Leake JR, Pressel S (2019) Functional complementarity of ancient 697
plant‐fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges 698
between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. New 699 Phytologist https://doi.org/10.1111/nph.15819 700
Field KJ, Cameron DD, Leake JR, Tille S, Bidartondo MI, Beerling DJ (2012) Contrasting 701 arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated 702 Palaeozoic CO2 decline. Nature Communications 3: 835 703
Field KJ, Pressel S (2018) Unity in diversity: structural and functional insights into the 704 ancient partnerships between plants and fungi. New Phytologist 220: 996–1011 705
Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI (2015a) Symbiotic 706 options for the conquest of land. Trends in Ecology & Evolution 30: 477-486 707
Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, 708 Duckett JG, Leake JR, Pressel S (2015b) First evidence of mutualism between 709 ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and 710 its response to simulated Palaeozoic changes in atmospheric CO2. New Phytologist 711 205: 743-756 712
Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, 713 Duckett JG, Leake JR, Pressel S (2016) Functional analysis of liverworts in dual 714 symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated 715 Palaeozoic CO2 decline. The ISME Journal 10: 1514-1526 716
Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and myco‐717
heterotrophic orchids provides insight into nitrogen and carbon gain from fungal 718 association. New Phytologist 160: 209-223 719
Gebauer G, Schulze E-D (1991) Carbon and nitrogen isotope ratios in different 720 compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, 721 NE Bavaria. Oecologia 87: 198-207 722
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large 723 phylogenies by maximum likelihood. Systematic Biology 52: 696-704 724
Hoysted GA, Kowal J, Jacob A, Rimington WR, Duckett JG, Pressel S, Orchard S, 725 Ryan MH, Field KJ, Bidartondo MI (2018) A mycorrhizal revolution. Current 726 Opinion in Plant Biology 44: 1-6 727
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, 728 Fraker E, Miadlikowska J (2006) Reconstructing the early evolution of Fungi using 729 a six-gene phylogeny. Nature 443: 818-822 730
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, 731 Cooper A, Markowitz S, Duran C (2012) Geneious Basic: an integrated and 732 extendable desktop software platform for the organization and analysis of sequence 733 data. Bioinformatics 28: 1647-1649 734
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 735 33 736
Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing 737 pieces. Current Opinion in Plant Biology 25: 115-122 738
Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007) An alternative mode 739 of early land plant colonization by putative endomycorrhizal fungi. Plant Signaling & 740 Behavior 2: 125-126 741
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis 742 version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870-1874 743
Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DG, Mu D, Pang E, Cao H, Cha H, Lin T 744 (2014) Single nucleus genome sequencing reveals high similarity among nuclei of an 745 endomycorrhizal fungus. PLoS Genetics 10: e1004078 746
Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang 747 Z, Schneider H, Donoghue PC (2018) The timescale of early land plant evolution. 748 Proceedings of the National Academy of Sciences: 201719588 749
Orchard S, Hilton S, Bending GD, Dickie IA, Standish RJ, Gleeson DB, Jeffery RP, 750 Powell JR, Walker C, Bass D (2017a) Fine endophytes (Glomus tenue) are related 751 to Mucoromycotina, not Glomeromycota. New Phytologist 213: 481-486 752
Orchard S, Standish RJ, Dickie IA, Renton M, Walker C, Moot D, Ryan MH (2017b) Fine 753 root endophytes under scrutiny: a review of the literature on arbuscule-producing 754 fungi recently suggested to belong to the Mucoromycotina. Mycorrhiza 27: 619-638 755
Pirozynski KA, Malloch DW (1975) The origin of land plants: A matter of mycotrophism. 756 Biosystems 6: 153-164 757
Press MC, Shah N, Tuohy JM, Stewart GR (1987) Carbon isotope ratios demonstrate 758 carbon flux from C4 host to C3 parasite. Plant Physiology 85: 1143-1145 759
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 760 289: 1920-1921 761
Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of 762 basal vascular plants: reopening a closed book? New Phytologist 205: 1394-1398 763
Rimington WR, Pressel S, Field KJ, Strullu‐Derrien C, Duckett JG, Bidartondo MI 764
(2016) Reappraising the origin of mycorrhizas. Molecular Mycorrhizal Symbiosis: 31-765 32 766
Ryan MH, Kirkegaard JA (2012) The agronomic relevance of arbuscular mycorrhizas in the 769 fertility of Australian extensive cropping systems. Agriculture, Ecosystems & 770 Environment 163: 37-53 771
Schmid E, Oberwinkler F (1993) Mycorrhiza‐like interaction between the achlorophyllous 772
gametophyte of Lycopodium clavatum L. and its fungal endophyte studied by light 773 and electron microscopy. New Phytologist 124: 69-81 774
Schulze E-D, Chapin FS, Gebauer G (1994) Nitrogen nutrition and isotope differences 775 among life forms at the northern treeline of Alaska. Oecologia 100: 406-412 776
Schulze E-D, Lange O, Ziegler H, Gebauer G (1991) Carbon and nitrogen isotope ratios of 777 mistletoes growing on nitrogen and non-nitrogen fixing hosts and on CAM plants in 778 the Namib desert confirm partial heterotrophy. Oecologia 88: 457-462 779
Smith SE, Anderson IC, Smith FA (2015) Mycorrhizal associations and phosphorus 780 acquisition: from cells to ecosystems. Annual Plant Reviews Online 48: 409-440 781
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: 782 new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 783 62: 227-250 784
Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million 786 year old) closely resemble those in extant lower land plants: novel insights into 787 ancestral plant–fungus symbioses. New Phytologist 203: 964-979 788
von Oheimb G, Power SA, Falk K, Friedrich U, Mohamed A, Krug A, Boschatzke N, 789 Härdtle W (2010) N: P ratio and the nature of nutrient limitation in Calluna-dominated 790 heathlands. Ecosystems 13: 317-327 791
Walker C, Gollotte A, Redecker D (2018) A new genus, Planticonsortium 792 (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, 793 Glomus tenue (basionym Rhizophagus tenuis). Mycorrhiza: 1-7 794
Parsed CitationsAlbornoz FE, Lambers H, Turner BL, Teste FP, Laliberté E (2016) Shifts in symbiotic associations in plants capable of forming multipleroot symbioses across a long‐term soil chronosequence. Ecology and Evolution 6: 2368-2377
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124: 949-958Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ (2004) Changing partners in the dark: isotopic and molecular evidence ofectomycorrhizal liaisons between forest orchids and trees. Proceedings of the Royal Society of London B: Biological Sciences 271:1799-1806
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. BiologyLetters: rsbl20101203
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Brundrett M, Bougher N, Dell B, Grove T (1996) Working with Mycorrhizas in Forestry and Agriculture.
Cameron DD, Johnson I, Leake JR, Read DJ (2007) Mycorrhizal acquisition of inorganic phosphorus by the green-leaved terrestrialorchid Goodyera repens. Annals of Botany 99: 831-834
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfersin the green‐leaved terrestrial orchid Goodyera repens. New Phytologist 171: 405-416
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS (2009) Whyare non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of currenthypotheses. Functional Plant Biology 36: 199-213
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annual Review of Ecology andSystematics 33: 507-559
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Desirò A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses in hornworts: a chequered history. Proceedingsof the Royal Society of London B: Biological Sciences 280: 20130207
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Duckett JG, Carafa A, Ligrone R (2006) A highly differentiated glomeromycotean association with the mucilage-secreting, primitiveantipodean liverwort Treubia (Treubiaceae): clues to the origins of mycorrhizas. American Journal of Botany 93: 797-813
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Duckett JG, Ligrone R (1992) A light and electron microscope study of the fungal endophytes in the sporophyte and gametophyte ofLycopodium cernuum with observations on the gametophyte–sporophyte junction. Canadian Journal of Botany 70: 58-72
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Edgar R (2016) UCHIME2: improved chimera prediction for amplicon sequencing. bioRxiv: 074252Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Biology 40:503-537
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Farquhar GD, O'Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbondioxide concentration in leaves. Functional Plant Biology 9: 121-137
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2019) Functionalcomplementarity of ancient plant‐fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges betweenMucoromycotina and Glomeromycotina fungal symbionts of liverworts. New Phytologist https://doi.org/10.1111/nph.15819
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Field KJ, Cameron DD, Leake JR, Tille S, Bidartondo MI, Beerling DJ (2012) Contrasting arbuscular mycorrhizal responses of vascularand non-vascular plants to a simulated Palaeozoic CO2 decline. Nature Communications 3: 835
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Field KJ, Pressel S (2018) Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi.New Phytologist 220: 996–1011
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI (2015a) Symbiotic options for the conquest of land. Trends in Ecology &Evolution 30: 477-486
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2015b) Firstevidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response tosimulated Palaeozoic changes in atmospheric CO2. New Phytologist 205: 743-756
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2016) Functionalanalysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. TheISME Journal 10: 1514-1526
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and myco‐heterotrophic orchids provides insight intonitrogen and carbon gain from fungal association. New Phytologist 160: 209-223
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Gebauer G, Schulze E-D (1991) Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abiesforest in the Fichtelgebirge, NE Bavaria. Oecologia 87: 198-207
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. SystematicBiology 52: 696-704
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hoysted GA, Kowal J, Jacob A, Rimington WR, Duckett JG, Pressel S, Orchard S, Ryan MH, Field KJ, Bidartondo MI (2018) Amycorrhizal revolution. Current Opinion in Plant Biology 44: 1-6
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J (2006) Reconstructingthe early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-822
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) GeneiousBasic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 33Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Current Opinion in Plant Biology25: 115-122
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007) An alternative mode of early land plant colonization by putative
endomycorrhizal fungi. Plant Signaling & Behavior 2: 125-126Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. MolecularBiology and Evolution 33: 1870-1874
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DG, Mu D, Pang E, Cao H, Cha H, Lin T (2014) Single nucleus genome sequencingreveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genetics 10: e1004078
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PC (2018) Thetimescale of early land plant evolution. Proceedings of the National Academy of Sciences: 201719588
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Orchard S, Hilton S, Bending GD, Dickie IA, Standish RJ, Gleeson DB, Jeffery RP, Powell JR, Walker C, Bass D (2017a) Fineendophytes (Glomus tenue) are related to Mucoromycotina, not Glomeromycota. New Phytologist 213: 481-486
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Orchard S, Standish RJ, Dickie IA, Renton M, Walker C, Moot D, Ryan MH (2017b) Fine root endophytes under scrutiny: a review of theliterature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina. Mycorrhiza 27: 619-638
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Pirozynski KA, Malloch DW (1975) The origin of land plants: A matter of mycotrophism. Biosystems 6: 153-164Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Press MC, Shah N, Tuohy JM, Stewart GR (1987) Carbon isotope ratios demonstrate carbon flux from C4 host to C3 parasite. PlantPhysiology 85: 1143-1145
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289: 1920-1921Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of basal vascular plants: reopening a closed book?New Phytologist 205: 1394-1398
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rimington WR, Pressel S, Field KJ, Strullu‐Derrien C, Duckett JG, Bidartondo MI (2016) Reappraising the origin of mycorrhizas.Molecular Mycorrhizal Symbiosis: 31-32
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ryan MH, Kirkegaard JA (2012) The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive croppingsystems. Agriculture, Ecosystems & Environment 163: 37-53
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schmid E, Oberwinkler F (1993) Mycorrhiza‐like interaction between the achlorophyllous gametophyte of Lycopodium clavatum L. andits fungal endophyte studied by light and electron microscopy. New Phytologist 124: 69-81
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schulze E-D, Chapin FS, Gebauer G (1994) Nitrogen nutrition and isotope differences among life forms at the northern treeline ofAlaska. Oecologia 100: 406-412
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schulze E-D, Lange O, Ziegler H, Gebauer G (1991) Carbon and nitrogen isotope ratios of mistletoes growing on nitrogen and non-nitrogen fixing hosts and on CAM plants in the Namib desert confirm partial heterotrophy. Oecologia 88: 457-462
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Smith SE, Anderson IC, Smith FA (2015) Mycorrhizal associations and phosphorus acquisition: from cells to ecosystems. Annual PlantReviews Online 48: 409-440
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystemscales. Annual Review of Plant Biology 62: 227-250
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Strullu‐Derrien C, Kenrick P, Pressel S, Duckett JG, Rioult JP, Strullu DG (2014) Fungal associations in Horneophyton ligneri from theRhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungussymbioses. New Phytologist 203: 964-979
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
von Oheimb G, Power SA, Falk K, Friedrich U, Mohamed A, Krug A, Boschatzke N, Härdtle W (2010) N: P ratio and the nature of nutrientlimitation in Calluna-dominated heathlands. Ecosystems 13: 317-327
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Walker C, Gollotte A, Redecker D (2018) A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fineroot endophyte, Glomus tenue (basionym Rhizophagus tenuis). Mycorrhiza: 1-7
Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title