Experimental Evidence of Microbial Inheritance in Plants and Transmission Routes from Seed to Phyllosphere and Root

Abstract

Abstract Background While the environment is considered the primary origin for establishing the microbiome of newly developing plants, the potential role of seeds as a source of transmitting microorganisms has not received much attention. Here we tested the hypothesis that the plant microbiome is at least partially inherited through vertical transmission. We investigated where microbes reside within a seed, and how microbes are subsequently transmitted from the seed to seedling’s belowground and aboveground plant tissues. To this aim, an experimental culturing device was constructed to grow oak seedlings in a microbe-free environment while keeping the belowground and aboveground tissues separated.Results Amplicon sequencing of fungal ITS2 and bacterial 16S rDNA revealed that the seed microbiome is diverse and non-randomly distributed within an acorn. The large majority (> 95%) of fungi and bacteria present in the acorn were transmitted to the seedling. The microbial composition of the phyllosphere strongly resembled the composition found in the embryo, whereas the roots and pericarp each had a distinct microbial community. Similar relationships were observed for both fungi and bacteria.Conclusion Our findings demonstrate a high level of microbial diversity and spatial partitioning of the fungal and bacterial community within both seed and seedling, indicating inheritance, niche differentiation, and divergent transmission routes for the establishment of root and phyllosphere communities in oak seedlings. The study provides new information on the importance of the maternal environment as a source of the seedling microbiome, with significant implications for our understanding of the continuity of the plant microbiome across generations.