Abstract

BackgroundPlants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host. This microbiota can thus be considered a toolbox enabling plants to buffer local environmental changes, with a positive influence on plant fitness. In this context, the transmission of the microbiota to the progeny represent a way to ensure the presence of beneficial symbionts within the habitat. Examples of such transmission have been mainly described for seed transmission and concern a few pathogenic microorganisms. We investigated the transmission of symbiotic partners to plant progeny within clonal plant network.MethodsWe used the clonal plant Glechoma hederacea as plant model and forced newly emitted clonal progeny to root in separated pots while controlling the presence of microorganisms. We used an amplicon sequencing approach of 16S and 18S rRNA targeting bacteria/archaea and fungi respectively to describe the root microbiota of mother and clonal-plant offspring.ResultsWe demonstrated the vertical transmission of a significant proportion of the mother plants’ symbiotic bacteria and fungi to the daughters. Interestingly, archaea were not transmitted to the daughter plants. Transmitted communities had lower richness, suggesting a filtration during transmission. We found that the transmitted pool of microorganisms was similar among daughters, constituting the heritability of a specific cohort of microorganisms, opening a new understanding of the plant holobiont. We also found significant effects of distance to the mother plant and of growth time on the richness of the microbiota transmitted.ConclusionsIn this clonal plant, microorganisms are transmitted between individuals through connections, thereby ensuring the availability of microbe partners for the newborn plants as well as the dispersion between hosts for the microorganisms. This previously undescribed ecological process allows the dispersal of microorganisms in space and across plant generations. As the vast majority of plants are clonal, this process might be therefore a strong driver of ecosystem functioning and assembly of plant and microorganism communities in a wide range of ecosystems.

Highlights

  • Plants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host

  • Archaea were not detected in the daughter ramets, but fungi and bacteria were found in daughter roots (Fig. 2)

  • To test whether this observed heritability was higher than would be expected stochastically, we used a null model approach in which the identity of the fungi or bacteria species in the experimental samples was randomized while keeping the operational taxonomic units (OTUs) richness identical

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Summary

Introduction

Plants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host This microbiota can be considered a toolbox enabling plants to buffer local environmental changes, with a positive influence on plant fitness. All living plants experience interactions with endophytic microorganisms and are known to harbor a great diversity of symbionts (i.e., long-lasting interactions) including fungi [1, 2], bacteria [3,4,5], and archaea [6] which collectively form the plant microbiota This microbiota performs ecological functions that extend the plant’s ability to adapt to environmental conditions [7, 8]. Some studies have evidenced a vertical inheritance of endophytic symbionts colonizing host plants through the seeds: the most wellknown example is perhaps the transmission of the stressprotective endophyte Neotyphodium coenocephalum to the descendants in several grass plant species [19, 20]

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