Browse by volume Browse by section Browse by topic Browse by conference

Section: Microbiology
Topic: Microbiology, Biology of interactions, Plant biology

Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype

Simonin, Marie1  ; Préveaux, Anne1; Marais, Coralie1; Garin, Tiffany1; Arnault, Gontran1 ; Sarniguet, Alain1 ; Barret, Matthieu1 
1 Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, F-49000 Angers, France

10.24072/pcjournal.329 - Peer Community Journal, Volume 3 (2023), article no. e95.

Get full text PDF Peer reviewed and recommended by PCI

Seed-borne microorganisms can be pioneer taxa during germination and seedling emergence. Still, the identity and phenotypic effects of these taxa that constitute a primary inoculum of plant microbiota is mostly unknown. Here, we studied the transmission of bacteria from radish seeds to seedlings using the inoculation of individual seed-borne strains and synthetic communities (SynComs) under  in vitro conditions. The SynComs were composed of highly abundant and prevalent, sub-dominant, or rare bacterial seed taxa. We monitored the transmission of each strain alone or in communities using gyrB gene amplicon sequencing and assessed their impacts on germination and seedling phenotype. All strains and SynComs successfully colonized seedlings and we were able to reconstruct a richness gradient (6, 8 and 12 strains) on both seeds and seedlings. Stenotrophomonas rhizophila became dominant on seedlings of the three SynComs but most strains had variable transmission success (i.e increasing, stable or decreasing during seed to seedling transition) that also depended on the SynCom richness. Most individual strains had no effect on seedling phenotypes, with the exception of Pseudomonas viridiflava and Paenibacillus sp. which had detrimental effects on germination and seedling development. Abnormal seedling morphologies were also observed with SynComs but their proportions decreased at the highest richness level. Interestingly, some bacterial strains previously identified as core taxa of radish seeds (Pseudomonas viridiflava,  Erwinia persicina) were associated with detrimental effects on seedling phenotypes either in isolation or in SynComs. These results confirm that the plant core microbiome includes pathogenic and not only commensal or mutualistic taxa. Altogether, these results show that SynCom inoculation can effectively manipulate seed and seedling microbiota diversity and thus represents a promising tool to better understand the early stages of plant microbiota assembly. This study also highlights strong differences between native seed-borne taxa in the colonization and survival on plant habitats.

Published online:
DOI: 10.24072/pcjournal.329
Type: Research article
Keywords: Plant microbiota, Seed-borne bacteria, Core microbiota, Synthetic community, Phytobiome, Pathobiome
Simonin, Marie 1; Préveaux, Anne 1; Marais, Coralie 1; Garin, Tiffany 1; Arnault, Gontran 1; Sarniguet, Alain 1; Barret, Matthieu 1

1 Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, F-49000 Angers, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_329,
     author = {Simonin, Marie and Pr\'eveaux, Anne and Marais, Coralie and Garin, Tiffany and Arnault, Gontran and Sarniguet, Alain and Barret, Matthieu},
     title = {Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype},
     journal = {Peer Community Journal},
     eid = {e95},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.329},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.329/}
}
TY  - JOUR
AU  - Simonin, Marie
AU  - Préveaux, Anne
AU  - Marais, Coralie
AU  - Garin, Tiffany
AU  - Arnault, Gontran
AU  - Sarniguet, Alain
AU  - Barret, Matthieu
TI  - Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.329/
DO  - 10.24072/pcjournal.329
LA  - en
ID  - 10_24072_pcjournal_329
ER  - 
%0 Journal Article
%A Simonin, Marie
%A Préveaux, Anne
%A Marais, Coralie
%A Garin, Tiffany
%A Arnault, Gontran
%A Sarniguet, Alain
%A Barret, Matthieu
%T Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.329/
%R 10.24072/pcjournal.329
%G en
%F 10_24072_pcjournal_329
Simonin, Marie; Préveaux, Anne; Marais, Coralie; Garin, Tiffany; Arnault, Gontran; Sarniguet, Alain; Barret, Matthieu. Transmission of synthetic seed bacterial communities to radish seedlings: impact on microbiota assembly and plant phenotype. Peer Community Journal, Volume 3 (2023), article  no. e95. doi : 10.24072/pcjournal.329. https://peercommunityjournal.org/articles/10.24072/pcjournal.329/

Peer reviewed and recommended by PCI : 10.24072/pci.microbiol.100008

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Arnault, G.; Mony, C.; Vandenkoornhuyse, P. Plant microbiota dysbiosis and the Anna Karenina Principle, Trends in Plant Science, Volume 28 (2023) no. 1, pp. 18-30 | DOI

[2] Barret, M.; Briand, M.; Bonneau, S.; Préveaux, A.; Valière, S.; Bouchez, O.; Hunault, G.; Simoneau, P.; Jacques, M.-A. Emergence Shapes the Structure of the Seed Microbiota, Applied and Environmental Microbiology, Volume 81 (2015) no. 4, pp. 1257-1266 | DOI

[3] Bass, D.; Stentiford, G. D.; Wang, H.-C.; Koskella, B.; Tyler, C. R. The Pathobiome in Animal and Plant Diseases, Trends in Ecology & Evolution, Volume 34 (2019) no. 11, pp. 996-1008 | DOI

[4] Bintarti, A. F.; Sulesky-Grieb, A.; Stopnisek, N.; Shade, A. Endophytic Microbiome Variation Among Single Plant Seeds, Phytobiomes Journal, Volume 6 (2022) no. 1, pp. 45-55 | DOI

[5] Callahan, B. J.; McMurdie, P. J.; Rosen, M. J.; Han, A. W.; Johnson, A. J. A.; Holmes, S. P. DADA2: High-resolution sample inference from Illumina amplicon data, Nature Methods, Volume 13 (2016) no. 7, pp. 581-583 | DOI

[6] Carlström, C. I.; Field, C. M.; Bortfeld-Miller, M.; Müller, B.; Sunagawa, S.; Vorholt, J. A. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere, Nature Ecology & Evolution, Volume 3 (2019) no. 10, pp. 1445-1454 | DOI

[7] Chesneau, G.; Laroche, B.; Préveaux, A.; Marais, C.; Briand, M.; Marolleau, B.; Simonin, M.; Barret, M. Single Seed Microbiota: Assembly and Transmission from Parent Plant to Seedling, mBio, Volume 13 (2022) no. 6 | DOI

[8] Chesneau, G.; Torres-Cortes, G.; Briand, M.; Darrasse, A.; Preveaux, A.; Marais, C.; Jacques, M.-A.; Shade, A.; Barret, M. Temporal dynamics of bacterial communities during seed development and maturation, FEMS Microbiology Ecology, Volume 96 (2020) no. 12 | DOI

[9] DeFlaun, M. F.; Marshall, B. M.; Kulle, E.-P.; Levy, S. B. Tn 5 Insertion Mutants of Pseudomonas fluorescens Defective in Adhesion to Soil and Seeds, Applied and Environmental Microbiology, Volume 60 (1994) no. 7, pp. 2637-2642 | DOI

[10] Duque, E.; de la Torre, J.; Bernal, P.; Molina‐Henares, M. A.; Alaminos, M.; Espinosa‐Urgel, M.; Roca, A.; Fernández, M.; de Bentzmann, S.; Ramos, J. Identification of reciprocal adhesion genes in pathogenic and non‐pathogenic Pseudomonas, Environmental Microbiology, Volume 15 (2012) no. 1, pp. 36-48 | DOI

[11] Figueiredo dos Santos, L.; Fernandes Souta, J.; de Paula Soares, C.; Oliveira da Rocha, L.; Luiza Carvalho Santos, M.; Grativol, C.; Fernando Wurdig Roesch, L.; Lopes Olivares, F. Insights into the structure and role of seed-borne bacteriome during maize germination, FEMS Microbiology Ecology, Volume 97 (2021) no. 4 | DOI

[12] Finkel, O. M.; Salas-González, I.; Castrillo, G.; Conway, J. M.; Law, T. F.; Teixeira, P. J. P. L.; Wilson, E. D.; Fitzpatrick, C. R.; Jones, C. D.; Dangl, J. L. A single bacterial genus maintains root growth in a complex microbiome, Nature, Volume 587 (2020) no. 7832, pp. 103-108 | DOI

[13] Granato, E. T.; Meiller-Legrand, T. A.; Foster, K. R. The Evolution and Ecology of Bacterial Warfare, Current Biology, Volume 29 (2019) no. 11 | DOI

[14] Hibbing, M. E.; Fuqua, C.; Parsek, M. R.; Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle, Nature Reviews Microbiology, Volume 8 (2009) no. 1, pp. 15-25 | DOI

[15] Karasov, T. L.; Almario, J.; Friedemann, C.; Ding, W.; Giolai, M.; Heavens, D.; Kersten, S.; Lundberg, D. S.; Neumann, M.; Regalado, J.; Neher, R. A.; Kemen, E.; Weigel, D. Arabidopsis thaliana and Pseudomonas Pathogens Exhibit Stable Associations over Evolutionary Timescales, Cell Host & Microbe, Volume 24 (2018) no. 1 | DOI

[16] Kumar, M.; Kour, D.; Yadav, A. N.; Saxena, R.; Rai, P. K.; Jyoti, A.; Tomar, R. S. Biodiversity of methylotrophic microbial communities and their potential role in mitigation of abiotic stresses in plants, Biologia, Volume 74 (2019) no. 3, pp. 287-308 | DOI

[17] Kwak, M.-J.; Kong, H. G.; Choi, K.; Kwon, S.-K.; Song, J. Y.; Lee, J.; Lee, P. A.; Choi, S. Y.; Seo, M.; Lee, H. J.; Jung, E. J.; Park, H.; Roy, N.; Kim, H.; Lee, M. M.; Rubin, E. M.; Lee, S.-W.; Kim, J. F. Rhizosphere microbiome structure alters to enable wilt resistance in tomato, Nature Biotechnology, Volume 36 (2018) no. 11, pp. 1100-1109 | DOI

[18] Lahti, L.; Shetty, S.; Blake, T. Tools for microbiome analysis in R. Microbiome Package , Version 0.99, 88, 2012–2017, 2017

[19] Lamichhane, J. R.; Debaeke, P.; Steinberg, C.; You, M. P.; Barbetti, M. J.; Aubertot, J.-N. Abiotic and biotic factors affecting crop seed germination and seedling emergence: a conceptual framework, Plant and Soil, Volume 432 (2018) no. 1-2, pp. 1-28 | DOI

[20] Ling, N.; Huang, Q.; Guo, S.; Shen, Q. Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f.sp. niveum, Plant and Soil, Volume 341 (2010) no. 1-2, pp. 485-493 | DOI

[21] Lipps, S. M.; Samac, D. A. Pseudomonas viridiflava: An internal outsider of the Pseudomonas syringae species complex, Molecular Plant Pathology, Volume 23 (2021) no. 1, pp. 3-15 | DOI

[22] Lundberg, D. S.; de Pedro Jové, R.; Pramoj Na Ayutthaya, P.; Karasov, T. L.; Shalev, O.; Poersch, K.; Ding, W.; Bollmann-Giolai, A.; Bezrukov, I.; Weigel, D. Contrasting patterns of microbial dominance in the Arabidopsis thaliana phyllosphere, Proceedings of the National Academy of Sciences, Volume 119 (2022) no. 52 | DOI

[23] Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI

[24] Massart, S. Seed synthetic community matters and its impact on seedling is strain- and not species-dependant, Peer Community in Microbiology (2023) | DOI

[25] Masson, A.-S.; Ho Bich, H.; Simonin, M.; Nguyen Thi, H.; Czernic, P.; Moulin, L.; Bellafiore, S. Deep modifications of the microbiome of rice roots infected by the parasitic nematode Meloidogyne graminicola in highly infested fields in Vietnam, FEMS Microbiology Ecology, Volume 96 (2020) no. 7 | DOI

[26] Matsumoto, H.; Fan, X.; Wang, Y.; Kusstatscher, P.; Duan, J.; Wu, S.; Chen, S.; Qiao, K.; Wang, Y.; Ma, B.; Zhu, G.; Hashidoko, Y.; Berg, G.; Cernava, T.; Wang, M. Bacterial seed endophyte shapes disease resistance in rice, Nature Plants, Volume 7 (2021) no. 1, pp. 60-72 | DOI

[27] McMurdie, P. J.; Holmes, S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data, PLoS ONE, Volume 8 (2013) no. 4 | DOI

[28] Moroenyane, I.; Tremblay, J.; Yergeau, É. Soybean Microbiome Recovery After Disruption is Modulated by the Seed and Not the Soil Microbiome, Phytobiomes Journal, Volume 5 (2021) no. 4, pp. 418-431 | DOI

[29] Mundt, J. O.; Hinkle, N. F. Bacteria within ovules and seeds, Applied and Environmental Microbiology, Volume 32 (1976) no. 5, pp. 694-698 | DOI

[30] Newcombe, G.; Harding, A.; Ridout, M.; Busby, P. E. A Hypothetical Bottleneck in the Plant Microbiome, Frontiers in Microbiology, Volume 9 (2018) | DOI

[31] Oksanen, J.; Kindt, R.; Legendre, P.; O’Hara, B.; Stevens, M.; Oksanen, M.; Suggests, M. The vegan package. Community ecology package, 2007

[32] Pfeilmeier, S.; Petti, G. C.; Bortfeld-Miller, M.; Daniel, B.; Field, C. M.; Sunagawa, S.; Vorholt, J. A. The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves, Nature Microbiology, Volume 6 (2021) no. 7, pp. 852-864 | DOI

[33] Raja, K.; Anandham, R.; Sivasubramaniam, K. Infusing Microbial Consortia for Enhancing Seed Germination and Vigour in Pigeonpea (Cajanus cajan (L.) Millsp.), Current Science, Volume 117 (2019) no. 12 | DOI

[34] Rochefort, A.; Briand, M.; Marais, C.; Wagner, M.-H.; Laperche, A.; Vallée, P.; Barret, M.; Sarniguet, A. Influence of Environment and Host Plant Genotype on the Structure and Diversity of the Brassica napus Seed Microbiota, Phytobiomes Journal, Volume 3 (2019) no. 4, pp. 326-336 | DOI

[35] Rochefort, A.; Simonin, M.; Marais, C.; Guillerm-Erckelboudt, A.-Y.; Barret, M.; Sarniguet, A. Transmission of Seed and Soil Microbiota to Seedling, mSystems, Volume 6 (2021) no. 3 | DOI

[36] Rybakova, D.; Schmuck, M.; Wetzlinger, U.; Varo-Suarez, A.; Murgu, O.; Müller, H.; Berg, G. Kill or cure? The interaction between endophytic Paenibacillus and Serratia strains and the host plant is shaped by plant growth conditions, Plant and Soil, Volume 405 (2015) no. 1-2, pp. 65-79 | DOI

[37] Ryu, C.-M.; Kim, J.; Choi, O.; Kim, S. H.; Park, C. S. Improvement of biological control capacity of Paenibacillus polymyxa E681 by seed pelleting on sesame, Biological Control, Volume 39 (2006) no. 3, pp. 282-289 | DOI

[38] Samad, A.; Antonielli, L.; Sessitsch, A.; Compant, S.; Trognitz, F. Comparative genome analysis of the vineyard weed endophyte Pseudomonas viridiflava CDRTc14 showing selective herbicidal activity, Scientific Reports, Volume 7 (2017) no. 1 | DOI

[39] Shakya, D. D.; Vinther, F. Occurrence of Pseudomonas viridiflava in Seedlings of Radish, Journal of Phytopathology, Volume 124 (2013) no. 2, pp. 123-127 | DOI

[40] Shalev, O.; Karasov, T. L.; Lundberg, D. S.; Ashkenazy, H.; Pramoj Na Ayutthaya, P.; Weigel, D. Commensal Pseudomonas strains facilitate protective response against pathogens in the host plant, Nature Ecology & Evolution, Volume 6 (2022) no. 4, pp. 383-396 | DOI

[41] Simonin M Script - Code for bioinformatics and Figures of Simonin et al. 2023 PCI Microbiol (Version 1), Zenodo, 2023 | DOI

[42] Simonin, M.; Briand, M.; Chesneau, G.; Rochefort, A.; Marais, C.; Sarniguet, A.; Barret, M. Seed microbiota revealed by a large‐scale meta‐analysis including 50 plant species, New Phytologist, Volume 234 (2022) no. 4, pp. 1448-1463 | DOI

[43] Simonin, M.; Dasilva, C.; Terzi, V.; Ngonkeu, E. L. M.; Diouf, D.; Kane, A.; Béna, G.; Moulin, L. Influence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a core microbiome across eight African and European soils, FEMS Microbiology Ecology, Volume 96 (2020) no. 6 | DOI

[44] Torres-Cortés, G.; Bonneau, S.; Bouchez, O.; Genthon, C.; Briand, M.; Jacques, M.-A.; Barret, M. Functional Microbial Features Driving Community Assembly During Seed Germination and Emergence, Frontiers in Plant Science, Volume 9 (2018) | DOI

[45] Torres-Cortés, G.; Garcia, B. J.; Compant, S.; Rezki, S.; Jones, P.; Préveaux, A.; Briand, M.; Roulet, A.; Bouchez, O.; Jacobson, D.; Barret, M. Differences in resource use lead to coexistence of seed-transmitted microbial populations, Scientific Reports, Volume 9 (2019) no. 1 | DOI

[46] Truyens, S.; Weyens, N.; Cuypers, A.; Vangronsveld, J. Bacterial seed endophytes: genera, vertical transmission and interaction with plants, Environmental Microbiology Reports, Volume 7 (2014) no. 1, pp. 40-50 | DOI

[47] Vogel, C. M.; Potthoff, D. B.; Schäfer, M.; Barandun, N.; Vorholt, J. A. Protective role of the Arabidopsis leaf microbiota against a bacterial pathogen, Nature Microbiology, Volume 6 (2021) no. 12, pp. 1537-1548 | DOI

[48] Walsh, C. M.; Becker-Uncapher, I.; Carlson, M.; Fierer, N. Variable influences of soil and seed-associated bacterial communities on the assembly of seedling microbiomes, The ISME Journal, Volume 15 (2021) no. 9, pp. 2748-2762 | DOI

[49] Wang, Q.; Garrity, G. M.; Tiedje, J. M.; Cole, J. R. Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy, Applied and Environmental Microbiology, Volume 73 (2007) no. 16, pp. 5261-5267 | DOI

[50] Wang, N. R.; Wiesmann, C. L.; Melnyk, R. A.; Hossain, S. S.; Chi, M.-H.; Martens, K.; Craven, K.; Haney, C. H. Commensal Pseudomonas fluorescens Strains Protect Arabidopsis from Closely Related Pseudomonas Pathogens in a Colonization-Dependent Manner, mBio, Volume 13 (2022) no. 1 | DOI

[51] Yousef-Coronado, F.; Travieso, M. L.; Espinosa-Urgel, M. Different, overlapping mechanisms for colonization of abiotic and plant surfaces by Pseudomonas putida, FEMS Microbiology Letters, Volume 288 (2008) no. 1, pp. 118-124 | DOI

Cited by Sources: