Manipulation of in planta ethylene levels modulates the metabolome of Populus tremula x tremuloides in a microbial-dependent manner.

Abstract

BackgroundThe assembly of tree microbiota is a dynamic process that varies across space and time, influenced by both biotic and abiotic factors. Plants have developed defence strategies, mediated by phytohormones such as ethylene, to manage its interactions with pathogens and, in certain non-perennials, interactions with the commensal microbiota. However, whether and how ethylene regulation affects the assembly of tree microbiota is unknown. ResultsWe investigated the assembly of fungal and bacterial communities in poplars (P. tremula x. P. tremuloides T89), altered either in ethylene biosynthesis (ACO1), or in ethylene perception (etr1.1), by combining high-throughput amplicon sequencing with confocal microscopy. In parallel, we characterised root exudates, as well as root and shoot metabolomes of the different poplar lines grown on sterile soil and in the presence of microbiota using GC-MS. Alteration of ethylene levels had little impact on the metabolome of sterile poplars, but led to differential primary and secondary metabolic responses in the root and shoots of poplars colonised by microorganisms. These metabolomic changes were associated with a decrease in fungal colonisation of shoots, particularly by saprophytes in the early stages, whereas reduced ethylene stimulated root colonisation by fungi. Conversely, arbuscular mycorrhizal fungal and bacterial communities, as well as root exudation, were little affected by changes in ethylene production. ConclusionThe findings of this study suggest a potential dual role for ethylene in poplar, whereby its levels may either promote or inhibit microbial growth and activity, depending on the concentration, microbial trophic guild, and poplar organ.