A Hypothetical Bottleneck in the Plant Microbiome

Newcombe, George; Harding, A. J.; Ridout, Mary; Busby, Posy E.

doi:10.3389/fmicb.2018.01645

Cited by 76 publications

(80 citation statements)

References 72 publications

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“…The present study demonstrated that individual seeds possessed high microbial diversity, that was higher in the embryo than in the pericarp. These results are in contrast to other recent studies that reported a limited number of bacterial and/or fungal species present in seeds [12,13].…”

Section: Discussioncontrasting

confidence: 99%

“…The majority of previous studies on the seed microbiome used bulk samples (several pooled seeds) [4,17,51] which in ates microbial diversity, especially when evaluating the transmission of the inherited microbiome into individual seeds [12,21]. The present study demonstrated that individual seeds possessed high microbial diversity, that was higher in the embryo than in the pericarp.…”

Section: Discussionmentioning

confidence: 49%

“…While information on the seed microbiome is sparse relative to data on the rhizosphere and phyllosphere, the studies that have been conducted have reported contradictory results. Some studies indicate that surface sterilization was enough to obtain microbe-free seeds [10,11], while others found a very limited number of microbes [12,13] to high microbial diversity [14][15][16][17] retained in surface-sterilized seeds. Regardless of the number of potential species, different seed tissues (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…Panel a shows the process of vertical transmission, with the hypothesized bottleneck at the seed-level. Several studies have explored how microbes move from the parent tree into the seed[12,51], but we lack studies on the transmission from the seed to the seedling. Panel b shows a hypothetical Venn diagram illustrating the categorization of the seed microbiome into the transient (pink) and transmitted (green) microbiome.…”

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confidence: 99%

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

Abdelfattah

Wisniewski

Schena

et al. 2020

Preprint

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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.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 49%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Abdelfattah

Wisniewski

Schena

et al. 2020

Preprint

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“…This may occur via 'priority effects' [64] mediated by the local conditions. Also referred to as the primary symbiont hypothesis, these effects have been reported in plants: bottlenecks in endophyte diversity associated with individual plant seeds are proposed to impact subsequent plant microbiome diversity [65].…”

Section: More Diverse Communities Of Symbiontsmentioning

confidence: 99%

The Pathobiome in Animal and Plant Diseases

Bass

Stentiford

Wang

et al. 2019

Trends in Ecology & Evolution

258

189

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A growing awareness of the diversity and ubiquity of microbes (eukaryotes, prokaryotes, and viruses) associated with larger 'host' organisms has led to the realisation that many diseases thought to be caused by one primary agent are the result of interactions between multiple taxa and the host. Even where a primary agent can be identified, its effect is often moderated by other symbionts. Therefore, the one pathogen-one disease paradigm is shifting towards the pathobiome concept, integrating the interaction of multiple symbionts, host, and environment in a new understanding of disease aetiology. Taxonomically, pathobiomes are variable across host species, ecology, tissue type, and time. Therefore, a more functionally driven understanding of pathobiotic systems is necessary, based on gene expression, metabolic interactions, and ecological processes. Disease in a Microbe-Dominated World The pathobiome (see Glossary) concept arose from human studies in which disruption of a healthpromoting and ecologically stable gut microbiome resulted in dysbiosis: a microbiome community of low-diversity and modified metabolic state, exposing the gut to invasion by, and proliferation of, pathogenic agents [1,2]. Dysbiotic communities can subvert the immune system and lead to further deleterious effects [3]. This concept is being adopted for research into the pathology of other animals and plants because attempts to explain syndromic conditions by identifying a single pathogenic agent are often incomplete (i.e., the one pathogen-one disease paradigm is often insufficient to explain many diseases [4-6]). Pathobiomes differ from those assemblages representing healthy or 'normal' states. What is 'normal' likely encompasses a range of assemblages that need to be understood before a pathobiome can be reliably distinguished from them. There is a lack of consistency in defining 'pathobiome' in the literature, ranging from a single pathogenic agent interacting with its biotic and abiotic environments (e.g., [5]) to the effects of interacting communities of microbes on host health [7]. Our synthesis (Box 1) is based on the effects of multiple symbionts, across all domains of life, on host health. The term 'microbiome' generally excludes eukaryotes; therefore, in this review, we use the term 'symbiome' to describe the whole assemblage of associated organisms excluding the host, and 'symbiont' for individual taxa within that assemblage. This definition is concordant with an inclusive scheme of symbiosis acknowledged in [9], which ranges from neutralism (neutral effect on both partners) to mutual beneficial effects and mutual antagonistic effects, and all other possible combinations of neutral, beneficial, and antagonistic effects. The duration of the association need not necessarily be long-term, as interactions can be effective on even short timescales; great variability in duration of association is both possible and likely. This inclusive definition is not inconsistent with some previous usages of the term, and is required by the large div...

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