Abstract

Numerous plant pathogens, rhizosphere symbionts, and endophytic bacteria and yeasts produce the important phytohormone indole-3-acetic acid (IAA), often with profound effects on host plants. However, to date IAA production has not been documented among foliar endophytes -- the diverse guild of primarily filamentous Ascomycota that live within healthy, above-ground tissues of all plant species studied thus far. Recently bacteria that live within hyphae of endophytes (endohyphal bacteria) have been detected, but their effects have not been studied previously. Here we show not only that IAA is produced in vitro by a foliar endophyte (here identified as Pestalotiopsis aff. neglecta, Xylariales), but that IAA production is enhanced significantly when the endophyte hosts an endohyphal bacterium (here identified as Luteibacter sp., Xanthomonadales). Both the endophyte and the endophyte/bacterium complex appear to rely on an L-tryptophan dependent pathway for IAA synthesis. The bacterium can be isolated from the fungus when the symbiotic complex is cultivated at 36°C. In pure culture the bacterium does not produce IAA. Culture filtrate from the endophyte-bacterium complex significantly enhances growth of tomato in vitro relative to controls and to filtrate from the endophyte alone. Together these results speak to a facultative symbiosis between an endophyte and endohyphal bacterium that strongly influences IAA production, providing a new framework in which to explore endophyte-plant interactions.

Highlights

  • Diverse plant-associated microbes synthesize phytohormones such as gibberellins, cytokinins, jasmonic acid, abscisic acid, ethylene, and indole-3-acetic acid (IAA), often with profound effects on growth, tissue differentiation, and reproduction of their hosts [1,2,3,4,5,6,7,8]

  • Most examples of IAA production by plant-associated microbes come from plant pathogens, mycorrhizal fungi, rhizosphere endophytes, and bacteria and yeasts that are endophytic in above-ground tissues [14,15,16,17,18,19]

  • Neither 9143+ nor 9143- grew at 36 °C, but cultivation of 9143+ at this temperature resulted in successful isolation of the endohyphal bacterium

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Summary

Introduction

Diverse plant-associated microbes synthesize phytohormones such as gibberellins, cytokinins, jasmonic acid, abscisic acid, ethylene, and indole-3-acetic acid (IAA), often with profound effects on growth, tissue differentiation, and reproduction of their hosts [1,2,3,4,5,6,7,8]. IAA produced by fungi affiliated with plants can inhibit hypersensitive responses, reducing the production of defensive enzymes such as chitinase and glucanase (reviewed in 6) In both natural and human-made environments, plants consistently harbor filamentous fungi (primarily Pezizomycotina, Ascomycota) in their apparently healthy above-ground tissues [21]. These endophytes (Class 3, sensu [21]; hereafter, endophytes) are known from every major lineage of land plants in biomes ranging from tundra to tropical forests [22,23,24,25,26]. Endophytes often are closely related to pathogens, with transitions between endophytism and pathogenicity occurring frequently in the evolution of the Ascomycota [25]

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