Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism

Jason D. Hoeksema; James D. Bever; Sounak Chakraborty; V. Bala Chaudhary; Monique Gardes; Catherine A. Gehring; Miranda M. Hart; Elizabeth Ann Housworth; Wittaya Kaonongbua; John N. Klironomos; Marc J. Lajeunesse; James Meadow; Brook G. Milligan; Bridget J. Piculell; Anne Pringle; Megan A. Rúa; James Umbanhowar; Wolfgang Viechtbauer; Yen Wen Wang; Gail W.T. Wilson; Peter C. Zee

doi:10.1038/s42003-018-0120-9

Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism

Jason D. Hoeksema, James D. Bever, Sounak Chakraborty, V. Bala Chaudhary, Monique Gardes, Catherine A. Gehring, Miranda M. Hart, Elizabeth Ann Housworth, Wittaya Kaonongbua, John N. Klironomos, Marc J. Lajeunesse, James Meadow, Brook G. Milligan, Bridget J. Piculell, Anne Pringle, Megan A. Rúa, James Umbanhowar, Wolfgang Viechtbauer, Yen Wen Wang, Gail W.T. WilsonPeter C. Zee

Biological Sciences

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86 Scopus citations

Abstract

Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.

Original language	English (US)
Number of pages	1
Journal	Communications biology
Volume	1
DOIs	https://doi.org/10.1038/s42003-018-0120-9
State	Published - Jan 1 2018

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Hoeksema, J. D., Bever, J. D., Chakraborty, S., Chaudhary, V. B., Gardes, M., Gehring, C. A., Hart, M. M., Housworth, E. A., Kaonongbua, W., Klironomos, J. N., Lajeunesse, M. J., Meadow, J., Milligan, B. G., Piculell, B. J., Pringle, A., Rúa, M. A., Umbanhowar, J., Viechtbauer, W., Wang, Y. W., ... Zee, P. C. (2018). Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Communications biology, 1. https://doi.org/10.1038/s42003-018-0120-9

Hoeksema, JD, Bever, JD, Chakraborty, S, Chaudhary, VB, Gardes, M, Gehring, CA, Hart, MM, Housworth, EA, Kaonongbua, W, Klironomos, JN, Lajeunesse, MJ, Meadow, J, Milligan, BG, Piculell, BJ, Pringle, A, Rúa, MA, Umbanhowar, J, Viechtbauer, W, Wang, YW, Wilson, GWT & Zee, PC 2018, 'Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism', Communications biology, vol. 1. https://doi.org/10.1038/s42003-018-0120-9

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title = "Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism",

abstract = "Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.",

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AU - Bever, James D.

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AU - Chaudhary, V. Bala

AU - Gardes, Monique

AU - Gehring, Catherine A.

AU - Hart, Miranda M.

AU - Housworth, Elizabeth Ann

AU - Kaonongbua, Wittaya

AU - Klironomos, John N.

AU - Lajeunesse, Marc J.

AU - Meadow, James

AU - Milligan, Brook G.

AU - Piculell, Bridget J.

AU - Pringle, Anne

AU - Rúa, Megan A.

AU - Umbanhowar, James

AU - Viechtbauer, Wolfgang

AU - Wang, Yen Wen

AU - Wilson, Gail W.T.

AU - Zee, Peter C.

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N2 - Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.

AB - Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.

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Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism

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