A suite of rare microbes interacts with a dominant, heritable, fungal endophyte to influence plant trait expression

Authors: HARRISON, JOSHUA - University Of Wyoming; BELTRAN, LYRA - University Of Nevada; BUERKLE, C - University Of Wyoming; Cook, Daniel; Gardner, Dale; PARCHMAN, THOMAS - University Of Nevada; POULSON, SIMON - University Of Nevada; FORISTER, MATTHEW - University Of Nevada

Submitted to: The ISME Journal: Multidisciplinary Journal of Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2021
Publication Date: 3/31/2021
Citation: Harrison, J.G., Beltran, L.P., Buerkle, C.A., Cook, D., Gardner, D.R., Parchman, T.L., Poulson, S.R., Forister, M.L. 2021. A suite of rare microbes interacts with a dominant, heritable, fungal endophyte to influence plant trait expression . The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 15:2763-2778. https://doi.org/10.1038/s41396-021-00964-4.
DOI: https://doi.org/10.1038/s41396-021-00964-4

Interpretive Summary: Endophytes are microbes that live, for at least a portion of their life history, within plant tissues. Endophyte assemblages are often composed of a few abundant taxa and many infrequently-observed, low-biomass taxa that are, in a word, rare. The ways in which most endophytes affect host phenotype are unknown; however, certain dominant endophytes can influence plants in ecologically meaningful ways–including by affecting growth and immune system functioning. In contrast, the effects of rare endophytes on their hosts have been unexplored, including how rare endophytes might interact with abundant endophytes to shape plant phenotype. Here, we manipulate both the suite of rare foliar endophytes (including both fungi and bacteria) and Alternaria fulva – a vertically-transmitted and usually abundant fungus–within the fabaceous forb Astragalus lentiginosus. We report that rare, low-biomass endophytes affected host size and foliar %N, but only when the heritable fungal endophyte(A. fulva) was not present. A. fulva also reduced plant size and %N, but these deleterious effects on the host could be offset by a negative association we observed between this heritable fungus and a foliar pathogen. These results demonstrate how interactions among endophytic taxa determine the net effects on host plants and suggest that the myriad rare endophytes within plant leaves may be more than a collection of uninfluential, commensal organisms, but instead have meaningful ecological roles.

Technical Abstract: Endophytes are microbes that live, for at least a portion of their life history, within plant tissues. Endophyte assemblages are often composed of a few abundant taxa and many infrequently-observed, low-biomass taxa that are, in a word, rare. The ways in which most endophytes affect host phenotype are unknown; however, certain dominant endophytes can influence plants in ecologically meaningful ways–including by affecting growth and immune system functioning. In contrast, the effects of rare endophytes on their hosts have been unexplored, including how rare endophytes might interact with abundant endophytes to shape plant phenotype. Here, we manipulate both the suite of rare foliar endophytes (including both fungi and bacteria) and Alternaria fulva – a vertically-transmitted and usually abundant fungus–within the fabaceous forb Astragalus lentiginosus. We report that rare, low-biomass endophytes affected host size and foliar %N, but only when the heritable fungal endophyte(A. fulva) was not present. A. fulva also reduced plant size and %N, but these deleterious effects on the host could be offset by a negative association we observed between this heritable fungus and a foliar pathogen. These results demonstrate how interactions among endophytic taxa determine the net effects on host plants and suggest that the myriad rare endophytes within plant leaves may be more than a collection of uninfluential, commensal organisms, but instead have meaningful ecological roles.