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

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.

Microbial Flow Within an Air-Phyllosphere-Soil Continuum

“…Although there was a shared component of the microbial community in the soil, air, and phyllosphere, none of the shared microbes were dominant microbes, which suggests that plant microbes may be acquired inherently from seed ( Wulff et al, 2003 ; Vorholt, 2012 ). The results from a recent study (preprint) supports our point ( Abdelfattah et al, 2020 ). Thus, inheritance of microbes first from seeds and parent material and supplemented from the surrounding environment, such as the soil and air, may be the potential pathway to explain the origination of phyllosphere microbes ( Mukhopadhyay et al, 1996 ; Truyens et al, 2015 ; Cope-Selby et al, 2017 ).…”

Microbiome Modulation—Toward a Better Understanding of Plant Microbiome Response to Microbial Inoculants

“…The phyllosphere microbiome is also recruited from airborne dust or irrigation water ( Vorholt, 2012 ). Moreover, recent experimental evidences on the seed’s role in vertical transmission across plant generations showed high 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 ( Rezki et al, 2016 ; Wassermann et al, 2019 ; Abdelfattah et al, 2021 ). Distinct microbes from the surrounding environment can colonize the plants surface and tissues, especially in the rhizosphere, which is the soil influenced by the plant root and as such the interface to the soil.…”

Factors contributing to ice nucleation and sequential freezing of leaves in wheat

“…Qiime2 (Bolyen et al 2019) was used for demultiplexing, merging, quality trimming of reads, acquired sequence variant (ASV) table generation, and rarefaction to account for uneven sequencing depth. Taxonomic clustering ASVs was done using a similarity threshold of 97% against the GreenGenes (DeSantis et al 2006) database for 16S reads and against the UNITE (Abarenkov et al 2010) database for ITS reads. MetagenomeSeq's Cumulative Sum Scaling (CSS) (Paulson et al 2013) was used as a normalization method subsequent to community composition analyses, including the calculation of Bray-Curtis dissimilarity metrics (Bray and Curtis 1957), the construction of PCoA plots, and PERMANOVA analyses.…”