Priority effects of wheat seed endophytes on a rhizosphere symbiosis

Ridout, Mary; Schroeder, Kurtis L.; Hunter, Samuel S.; Styer, J. Franklin; Newcombe, George

doi:10.1007/s13199-019-00606-6

Cited by 47 publications

(40 citation statements)

References 45 publications

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“…Historical contingency is mediated by priority effects that correspond to the impact of species on one another depending on its order of arrival within the local community (32). Importance of historical contingency in assembly of the plant microbiota was recently highlighted in wheat, where the identity of seed-transmitted fungal taxa can modify colonization of roots by dark septate endophytes, three weeks following germination (18). While we cannot conclude there is an absence of priority effects between microbial species within the root and stem microbial communities of B. napus, historical contingency is not promoted during seedling community assembly.…”

Section: Discussionmentioning

confidence: 99%

“…In spermatophyte, seed-associated microbial community constitutes the primary inoculum for the next plant generation (10). The seed microbiota can have a crucial role for crop installation by modulating dormancy (11,12), germination (13,14), seedling development (15–17) and recruitment of plant symbionts (18). Seed transmission of some specific plant-beneficial or phytopathogenic microbial strains is well documented (19–23).…”

Section: Introductionmentioning

confidence: 99%

“…The seed community is extremely reduced in terms of abundance compared to soil community, but its members have potentially a ‘home advantage’ as they have been selected by the plant. We therefore hypothesized that despite its lower microbial richness and diversity, seed microbiota being already present and more adapted to the plant environment, would benefit from priority effects over soil microbiota for the colonization of plant compartments (18). Nevertheless, adaptation to seed does probably not recover all features for adaptation to a growing seedling.…”

Section: Introductionmentioning

confidence: 99%

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Asymmetric outcome of community coalescence of seed and soil microbiota during early seedling growth

Rochefort

Simonin

Marais

et al. 2020

Preprint

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Seed microbial community constitutes a primary inoculum for plant microbiota assembly. Still, the persistence of seed microbiota when seeds encounter soil during plant emergence and early growth is barely documented. Here, we characterized the interchange event or coalescence of seed and soil microbiota and how it structured seedling bacterial and fungal communities. We performed eight contrasted coalescence events to identify drivers influencing seedling microbiota assembly: four seed lots of two Brassica napus genotypes were sown in two soils of contrasted diversity. We found that seedling root and stem microbiota were influenced by soil diversity but not by initial seed microbiota composition. A strong selection on the two-source communities occurred during microbiota assembly, with only 8-32% of soil taxa and 0.8-1.4% of seed-borne taxa colonizing seedlings. The recruitment of seedling microbiota came mainly from soil (35-72% of diversity) and not from seeds (0.3-15%). The outcome of seed and soil microbiota coalescence is therefore strongly asymmetrical with a dominance of soil taxa. Interestingly, seedling microbiota was primarily composed of initially rare taxa (from seed, soil or unknown origin) and sub-dominant soil taxa. Our results suggest that plant microbiome engineering success based on native seed or soil microbiota will rely on rare and sub-dominant taxa in source communities.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Asymmetric outcome of community coalescence of seed and soil microbiota during early seedling growth

Rochefort

Simonin

Marais

et al. 2020

Preprint

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“…1). To date, seed microbiome studies suggest that strict‐sense maternal microbiota transmission during floral and early seed development is relatively rare, as fresh seeds typically contain very few fungal species (Christian et al ., 2017; Sarmiento et al ., 2017; Ridout et al ., 2019). By contrast, Fort et al .…”

Section: Figmentioning

confidence: 99%

Oaks provide new perspective on seed microbiome assembly

U’Ren

Zimmerman

2021

New Phytologist

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“…The finding of P. agglomerans as a seed endophyte (e.g. in Eucaliptus (Ferreira et al, 2008), Rice (Ruiza et al, 2011) and wheat (Triticum aestivum) (Links et al, 2014;Díaz Herrera et al, 2016;Ridout et al, 2019)) and the ability of seed-borne P. agglomerans isolates to colonize the roots of seedlings upon germination (e.g. in Rice (Ruiza et al, 2011) and Wheat (Díaz Herrera et al, 2016)) suggest a role of the vertical transmission in the evolution of P. agglomerans association with plants.…”

Section: Introductionmentioning

confidence: 99%

Colonization dynamics of Pantoea agglomerans in the wheat root habitat

Soluch

Hülter

Picazo

et al. 2021

Environmental Microbiology

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Plants are colonized by microbial communities that have diverse implications for plant development and health. The establishment of a stable plant-bacteria interaction depends on a continuous coexistence over generations. Transmission via the seed is considered as the main route for vertical inheritance of plant-associated bacteria. Nonetheless, the ecological principles that govern the plant colonization by seed endophytes remain understudied. Here we quantify the contribution of arrival time and colonization history to bacterial colonization of the wheat root. Establishing a common seed endophyte, Pantoea agglomerans, and wheat as a model system enabled us to document bacterial colonization of the plant roots during the early stages of germination. Using our system, we estimate the carrying capacity of the wheat roots as 10 8 cells g −1 , which is robust among individual plants and over time. Competitions in planta reveal a significant advantage of early incoming colonizers over late-incoming colonizers. Priming for the wheat environment had little effect on the colonizer success. Our experiments thus provide empirical data on the root colonization dynamics of a seed endophyte. The persistence of seed endophyte bacteria with the plant population over generations may contribute to the stable transmission that is one route for the evolution of a stable host-associated lifestyle.

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Priority effects of wheat seed endophytes on a rhizosphere symbiosis

Cited by 47 publications

References 45 publications

Asymmetric outcome of community coalescence of seed and soil microbiota during early seedling growth

Asymmetric outcome of community coalescence of seed and soil microbiota during early seedling growth

Oaks provide new perspective on seed microbiome assembly

Colonization dynamics of Pantoea agglomerans in the wheat root habitat

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