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Herbivory enhances legume-rhizobia symbioses function, increasing aboveground allocation of biologically fixed nitrogen, but only in soils without additional nitrate

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Abstract

Purpose

Beneficial soil microbes, such as rhizobia, engage in facultative symbioses in the roots of leguminous host plants to exchange nitrogen for products of photosynthesis, and these symbioses can be altered by biotic and abiotic factors. Here, we investigated how soil nitrate supply and aboveground insect herbivory interact to influence biological nitrogen fixation in Medicago sativa (alfalfa or lucerne).

Methods

Using field and greenhouse experiments, we quantified above- and belowground allocation of rhizobially fixed nitrogen using isotopic nitrogen ratios in plants with different combinations of herbivory and nitrate supplementation. We caged Empoasca fabae (potato leafhopper) on fixing and non-fixing cultivars of M. sativa and supplemented soils with varied nitrate concentrations.

Results

We detected strong changes in legume above- and belowground allocation of fixed nitrogen in response to both herbivory and nitrate supply. Moderate nitrate soils, irrespective of herbivory, induced little to no fixed nitrogen allocation across both field and greenhouse experiments. In the field only, non-supplemented soil increased aboveground allocation of fixed nitrogen following herbivore damage but resulted in no changes belowground. In contrast, non-supplemented and high nitrate soils in the greenhouse increased above- and belowground fixed nitrogen allocation relative to moderate nitrate soils.

Conclusion

Our results demonstrate herbivory drives distinct plant allocation strategies across soil nitrate levels, advancing our understanding of how rhizobia influence legumes both above- and belowground. Herbivory-induced changes in rhizobia-legume symbioses are likely widespread across both agricultural and natural ecosystems.

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Acknowledgements

We are grateful to the Western Maryland Research and Education Center staff and greenhouse staff at the University of Maryland for their support and help in executing these experiments, as well as members of the Lamp Lab (Alina Avanesyan, Dylan Kutz, Kevin Clements, Kimmy Okada, Emily Mast, Nina McGranahan, Jessica Ho, Sami Louguit). We would like to thank Drs. Kelly Hamby, Daniel Gruner, and Karin Burghardt for feedback on an earlier version of this manuscript, as well as two anonymous reviewers. We also extend gratitude and appreciation to Dr. Alan Leslie for substantial guidance on statistical analyses and writing. This project was supported by a graduate research award provided to M. Thompson from Northeastern Sustainable Agriculture Research and Education (Award Number GNE18-187-32231), as well as by the Hatch Project MD-ENTM-180.

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  1. Department of Entomology, University of Maryland, College Park, 4291 Fieldhouse Drive, College Park, MD, 20742, USA

    Morgan N. Thompson & William O. Lamp

  2. Department of Entomology, Texas A&M University, TAMU 2475, College Station, TX, 77843-2475, USA

    Morgan N. Thompson

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Thompson, M.N., Lamp, W.O. Herbivory enhances legume-rhizobia symbioses function, increasing aboveground allocation of biologically fixed nitrogen, but only in soils without additional nitrate. Plant Soil 465, 301–316 (2021). https://doi.org/10.1007/s11104-021-04999-6

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  • DOI: https://doi.org/10.1007/s11104-021-04999-6

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