Single Seed Microbiota: Assembly and Transmission from Parent Plant to Seedling

Chesneau, Guillaume; Laroche, Béatrice; Préveaux, Anne; Marais, Coralie; Briand, Martial; Marolleau, Brice; Simonin, Marie; Barret, Matthieu

doi:10.1128/mbio.01648-22

Cited by 27 publications

(51 citation statements)

References 67 publications

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“…This variability in the assembly of seed microbiota has been reported by different studies and can be observed even at the single‐seed level (e.g. 2–28 bacterial ASVs per oak seed or 1–45 bacterial ASVs per bean seed) (Abdelfattah et al ., 2021; Chesneau et al ., 2021). However, the variability observed in this meta‐analysis also could be partly methodological because of the variable number of seeds used in different samples to characterize seed microbiota (from one to 1000 seeds).…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, this meta‐analysis included mainly seed microbiota characterization from multiple seeds (> 3 seeds in sample) with > 1000 reads. More work is needed at the single‐seed level (Abdelfattah et al ., 2021; Bintarti et al ., 2021; Chesneau et al ., 2021) to assess seed‐to‐seed variation and the proportion of seeds that do not have detectable microbiota (i.e. sterile seeds) (Newcombe et al ., 2018; Ridout et al ., 2019).…”

Section: Discussionmentioning

confidence: 99%

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Seed microbiota revealed by a large‐scale meta‐analysis including 50 plant species

et al. 2022

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Seed microbiota constitutes a primary inoculum for plants that is gaining attention owing to its role for plant health and productivity.Here, we performed a meta-analysis on 63 seed microbiota studies covering 50 plant species to synthesize knowledge on the diversity of this habitat.Seed microbiota are diverse and extremely variable, with taxa richness varying from one to thousands of taxa. Hence, seed microbiota presents a variable (i.e. flexible) microbial fraction but we also identified a stable (i.e. core) fraction across samples.Around 30 bacterial and fungal taxa are present in most plant species and in samples from all over the world. Core taxa, such as Pantoea agglomerans, Pseudomonas viridiflava, P. fluorescens, Cladosporium perangustum and Alternaria sp., are dominant seed taxa.The characterization of the core and flexible seed microbiota provided here will help uncover seed microbiota roles for plant health and design effective microbiome engineering.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Seed microbiota revealed by a large‐scale meta‐analysis including 50 plant species

et al. 2022

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“…A finer clustering method may be better suited to studying the transmission of seed-associated microbes into the spermosphere since genotypes originating from the seed may be grouped within 97% OTUs originating from the soil. We recognize microbes originating from the seed can colonize seedlings and other plant organs, which can alter plant health (Bintarti et al 2022b; Bintarti et al 2022a; Chesneau et al 2022; Chesneau et al 2020; Johnston-Monje et al 2016; Mitter et al 2017; Rochefort et al 2021; Shade et al 2017; Simonin et al 2022). For example, it was recently demonstrated that crop flowers sprayed with a beneficial bacterium can colonize endosperm and transmit to germinating seeds (Mitter et al 2017).…”

Section: Discussionmentioning

confidence: 99%

“…The spermosphere represents a critical zone for establishing vertically inherited seed microbes, and horizontal interactions between soil and seed-associated microbes (Chesneau et al 2022; Chesneau et al 2020; Rochefort et al 2021; Shade et al 2017; Simonin et al 2022). The outcome of these interactions can affect the life or death of the plant soon after sowing seeds (McKellar and Nelson 2003; Windstam and Nelson 2008).…”

Section: Introductionmentioning

confidence: 99%

Soybean and cotton spermosphere soil microbiome shows dominance of soil-borne copiotrophs

Olofintila

Noel

2023

Preprint

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The spermosphere is the transient, immediate zone of soil around imbibing and germinating seeds, rich in microbial activity. It represents a habitat where there is contact between seed-associated microbes and soil microbes, but is studied less compared to other plant habitats. Previous studies on spermosphere microbiology were primarily culture-based or did not sample the spermosphere soil as initially defined in space and time. Thus, the objectives of this study were to develop an efficient strategy to collect spermosphere soils around imbibing soybean and cotton in non-sterile soil and investigate factors contributing to changes in microbial communities. The method employed sufficiently collected spermosphere soil as initially defined in space (3-10 mm soil around a seed) by constraining the soil sampled with an cork borer and confining the soil to a 12-well microtiter plate. Spermosphere prokaryote composition changed over time and depended on the crop within six hours after seeds were sown. By 12 to 18 hours, crops had unique microbial communities in spermosphere soils. Prokaryote evenness dropped following seed imbibition and the proliferation of copiotroph soil bacteria in the phyla Proteobacteria and Firmicutes. Due to their long history of plant growth promotion, prokaryote OTUs in Bacillus, Paenibacillus, Burkholderia, Massilia, Azospirillum, and Pseudomonas were notable genera enriched in the cotton and soybean spermosphere. There was no consistent evidence that fungal communities changed like prokaryotes. However, fungi and prokaryotes were hub taxa in cotton and soybean spermosphere networks. Additionally, the enriched taxa were not hubs in networks, suggesting other taxa besides the copiotrophic may be important for spermosphere communities. Overall, this study advances knowledge in the assembly of the plant microbiome early in a plant's life, which may have plant health implications in more mature plant growth stages.

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“…In addition, seed microbiota functions should be considered: i.e. ecology, developmental stages, shaping of the core microbiota, vertical transmission [ 41 , 137 , 189 ], and seed-to-seed cycle [ 15 ]. Finally, an unexpected lack of reports on the effects of Arabidopsis microbiota/microbiome in issues such as nitrogen limitation [ 94 ], or plant–insect (nematode)-microbe interactions, is clearly a call for new studies.…”

Section: Concluding Remarks and Future Research Needsmentioning

confidence: 99%

The Arabidopsis holobiont: a (re)source of insights to understand the amazing world of plant–microbe interactions

Poupin

Ledger

Roselló-Móra

et al. 2023

Environmental Microbiome

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As holobiont, a plant is intrinsically connected to its microbiomes. However, some characteristics of these microbiomes, such as their taxonomic composition, biological and evolutionary role, and especially the drivers that shape them, are not entirely elucidated. Reports on the microbiota of Arabidopsis thaliana first appeared more than ten years ago. However, there is still a lack of a comprehensive understanding of the vast amount of information that has been generated using this holobiont. The main goal of this review was to perform an in-depth, exhaustive, and systematic analysis of the literature regarding the Arabidopsis–microbiome interaction. A core microbiota was identified as composed of a few bacterial and non-bacterial taxa. The soil (and, to a lesser degree, air) were detected as primary microorganism sources. From the plant perspective, the species, ecotype, circadian cycle, developmental stage, environmental responses, and the exudation of metabolites were crucial factors shaping the plant–microbe interaction. From the microbial perspective, the microbe-microbe interactions, the type of microorganisms belonging to the microbiota (i.e., beneficial or detrimental), and the microbial metabolic responses were also key drivers. The underlying mechanisms are just beginning to be unveiled, but relevant future research needs were identified. Thus, this review provides valuable information and novel analyses that will shed light to deepen our understanding of this plant holobiont and its interaction with the environment.

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Single Seed Microbiota: Assembly and Transmission from Parent Plant to Seedling

Abstract: Seeds are key components of plant fitness and are central to the sustainability of the agri-food system. Both the seed quality for food consumption and the seed vigor in agricultural settings can be influenced by the seed microbiota.

Cited by 27 publications

References 67 publications

Seed microbiota revealed by a large‐scale meta‐analysis including 50 plant species

Seed microbiota revealed by a large‐scale meta‐analysis including 50 plant species

Soybean and cotton spermosphere soil microbiome shows dominance of soil-borne copiotrophs

The Arabidopsis holobiont: a (re)source of insights to understand the amazing world of plant–microbe interactions

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