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

 
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Award ID(s):
1655726
NSF-PAR ID:
10485301
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
The ISME Journal
Volume:
15
Issue:
9
ISSN:
1751-7362
Format(s):
Medium: X Size: p. 2763-2778
Size(s):
["p. 2763-2778"]
Sponsoring Org:
National Science Foundation
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  1. null (Ed.)
    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. 
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  2. Summary

    Colonization by foliar endophytic fungi can affect the expression of host plant defenses and other ecologically important traits. However, whether endophyte colonization affects the uptake or redistribution of resources within and among host plant tissues remains unstudied.

    We inoculated leaves ofTheobroma cacaowith four common colonizers that range in their effect from protective to pathogenic (Colletotrichum tropicale,Pestalotiopsissp.,Colletotrichum theobromicola, orPhytophthora palmivora). We pulsed the soil with nitrogen‐15 (15N) and then traced15N uptake and its subsequent distribution to whole plants and individual leaves.

    At a whole‐plant level,C. tropicale‐inoculated plants showed significantly greater15N uptake than endophyte‐free plants did in the same pot. Among leaves within plants, younger leaves were particularly enriched in15N, but endophyte inoculation at the individual leaf level did not alter15N distribution within plants. However, leaves co‐inoculated with pathogenicPhytophthoraand protectiveC. tropicaleexperienced significantly elevated15N content as pathogen damage increased, compared with leaves inoculated only with the pathogen. Further, endophyte–pathogen co‐infection also increased total plant biomass.

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