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The interactive effects of plant microbial symbionts: a review and meta-analysis

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Abstract

In nature, plants often associate with multiple symbionts concurrently, yet the effects of tripartite symbioses are not well understood. We expected synergistic growth responses from plants associating with functionally distinct symbionts. In contrast, symbionts providing similar benefits to a host may reduce host plant growth. We reviewed studies investigating the effect of multiple interactions on host plant performance. Additionally, we conducted a meta-analysis on the studies that performed controlled manipulations of the presence of two microbial symbionts. Using response ratios, we investigated the effects on plants of pairs of symbionts (mycorrhizal fungi, fungal endophytes, and nitrogen-fixers). The results did not support the view that arbuscular mycorrhizal (AM) fungi and rhizobia should interact synergistically. In contrast, we found the joint effects of fungal endophytes and arbuscular mycorrhizal fungi to be greater than expected given their independent effects. This increase in plant performance only held for antagonistic endophytes, whose negative effects were alleviated when in association with AM fungi, while the impact of beneficial endophytes was not altered by infection with AM fungi. Generalizations from the meta-analysis were limited by the substantial variation within types of interactions and the data available, highlighting the need for more research on a range of plant systems.

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Acknowledgements

We thank Jason Hoeksema, the Bever and Clay lab groups, and two anonymous reviewers for insightful comments on this manuscript. We are grateful to the Indiana University Stat/Math Center for statistical help. We acknowledge the Indiana Academy of Sciences for funding support of this work.

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Authors and Affiliations

  1. Department of Biology, Indiana University, Jordan Hall, 1001 East Third Street, Bloomington, IN, 47405-3700, USA

    Anna L. Larimer, James D. Bever & Keith Clay

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  1. Anna L. Larimer
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  2. James D. Bever
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  3. Keith Clay
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Correspondence to Anna L. Larimer.

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Supporting Information 1

Articles reviewed (PDF 109 kb)

Supporting Information 2

Hedge’s d independent, overall, and interactive effect sizes (DOC 46 kb)

Supporting Information 3

Overall response ratios (PDF 45 kb)

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Larimer, A.L., Bever, J.D. & Clay, K. The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51, 139–148 (2010). https://doi.org/10.1007/s13199-010-0083-1

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