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Assembly of seed-associated microbial communities within and across successive plant generations

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Abstract

Background and aims

Seeds are involved in the transmission of microorganisms from one plant generation to another and consequently may act as the initial inoculum source for the plant microbiota. In this work, we assessed the structure and composition of the seed microbiota of radish (Raphanus sativus) across three successive plant generations.

Methods

Structure of seed microbial communities were estimated on individual plants through amplification and sequencing of genes that are markers of taxonomic diversity for bacteria (gyrB) and fungi (ITS1). The relative contribution of dispersal and ecological drift in inter-individual fluctuations were estimated with a neutral community model.

Results

Seed microbial communities of radish display a low heritability across plant generations. Fluctuations in microbial community profiles were related to changes in community membership and composition across plant generations, but also to variation between individual plants. Ecological drift was an important driver of the structure of seed bacterial communities, while dispersal was involved in the assembly of the fungal fraction of the seed microbiota.

Conclusions

These results provide a first glimpse of the governing processes driving the assembly of the seed microbiota.

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References

  • Abarenkov K, Nilsson R, Larsson K, Alexander I, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E, Pennanen T, Sen R, Taylor A, Tedersoo L, Ursing B, Vralstad T, Liimatainen K, Peintner U, Koljalg U (2010) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol 186:281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x

    Article  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Badri D, Zolla G, Bakker M, Manter D, Vivanco J (2013) Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198:264–273. https://doi.org/10.1111/nph.12124

    Article  CAS  PubMed  Google Scholar 

  • Barret M, Briand M, Bonneau S, Preveaux A, Valiere S, Bouchez O, Hunault G, Simoneau P, Jacques M (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81:1257–1266. https://doi.org/10.1128/AEM.03722-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sanchez-Garcia M, Ebersberger I, de Sousa F, Amend A, Jumpponen A, Unterseher M, Kristiansson E, Abarenkov K, Bertrand Y, Sanli K, Eriksson K, Vik U, Veldre V, Nilsson R (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919. https://doi.org/10.1111/2041-210X.12073.

    Google Scholar 

  • Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA (2014) A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet 10:e1004283

    Article  PubMed  PubMed Central  Google Scholar 

  • Buée M, Reich M, Murat C, Morin E, Nilsson R, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456. https://doi.org/10.1111/j.1469-8137.2009.03003.x

    Article  PubMed  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel N, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    Article  CAS  PubMed  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  PubMed  Google Scholar 

  • Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJ (2016) Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J 10:655–664

    Article  CAS  PubMed  Google Scholar 

  • Busby P, Ridout M, Newcombe G (2016) Fungal endophytes: modifiers of plant disease. Plant Mol Biol 90:645–655. https://doi.org/10.1007/s11103-015-0412-0

    Article  CAS  PubMed  Google Scholar 

  • Chee-Sanford JC, Williams II MM, Davis AS, Sims GK (2006) Do microorganisms influence seed-bank dynamics? Weed Sci 54:575–587

  • Classen A, Sundqvist M, Henning J, Newman G, Moore J, Cregger M, Moorhead L, Patterson C (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead? Ecosphere 6:1–21. https://doi.org/10.1890/ES15-00217.1

  • Compant S, van der Heijden M, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214. https://doi.org/10.1111/j.1574-6941.2010.00900.x

    CAS  PubMed  Google Scholar 

  • Dombrowski N, Schlaeppi K, Agler MT, Hacquard S, Kemen E, Garrido-Oter R, Wunder J, Coupland G, Schulze-Lefert P (2017) Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME J 11:43–55

    Article  CAS  PubMed  Google Scholar 

  • Edgar R (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  • Edgar R, Haas B, Clemente J, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112:911–920

    Article  Google Scholar 

  • Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23

    Article  Google Scholar 

  • Goggin DE, Emery RJ, Kurepin LV, Powles SB (2015) A potential role for endogenous microflora in dormancy release, cytokinin metabolism and the response to fluridone in Lolium rigidum seeds. Ann Bot 115:293–301

    Article  PubMed  Google Scholar 

  • Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S, Campisano A, Doring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Hodgson S, de Cates C, Hodgson J, Morley N, Sutton B, Gange A (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208. https://doi.org/10.1002/ece3.953

    Article  PubMed  PubMed Central  Google Scholar 

  • Horton M, Bodenhausen N, Beilsmith K, Meng D, Muegge B, Subramanian S, Vetter M, Vilhjalmsson B, Nordborg M, Gordon J, Bergelson J (2014) Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat Commun 5:5320

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klaedtke S, Jacques M, Raggi L, Preveaux A, Bonneau S, Negri V, Chable V, Barret M (2016) Terroir is a key driver of seed-associated microbial assemblages. Environ Microbiol 18:1792–1804. https://doi.org/10.1111/1462-2920.12977

    Article  CAS  PubMed  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lau J, Lennon J (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci U S A 109:14058–14062. https://doi.org/10.1073/pnas.1202319109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Links M, Demeke T, Grafenhan T, Hill J, Hemmingsen S, Dumonceaux T (2014) Simultaneous profiling of seed-associated bacteria and fungi reveals antagonistic interactions between microorganisms within a shared epiphytic microbiome on Triticum and Brassica seeds. New Phytol 202:542–553. https://doi.org/10.1111/nph.12693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Velasco G, Carder P, Welbaum G, Ponder M (2013) Diversity of the spinach (Spinacia oleracea) spermosphere and phyllosphere bacterial communities. FEMS Microbiol Lett 346:146–154. https://doi.org/10.1111/1574-6968.12216

    Article  CAS  PubMed  Google Scholar 

  • Lumactud R, Shen SY, Lau M, Fulthorpe R (2016) Bacterial endophytes isolated from plants in natural oil seep soils with chronic hydrocarbon contamination. Front Microbiol 7:755

    Article  PubMed  PubMed Central  Google Scholar 

  • Lumactud R, Fulthorpe R, Sentchilo V, van der Meer JR (2017) Draft genome sequence of Plantibacter flavus strain 251 isolated from a plant growing in a chronically hydrocarbon-contaminated site. Genome Announc 5:e00276–e00217

    PubMed  PubMed Central  Google Scholar 

  • Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, dela Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lymperopoulou D, Adams R, Lindow S (2016) Contribution of vegetation to the microbial composition of nearby outdoor air. Appl Environ Microbiol 82:3822–3833. https://doi.org/10.1128/AEM.00610-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maignien L, DeForce E, Chafee M, Eren A, Simmons S (2014) Ecological succession and stochastic variation in the assembly of arabidopsis thaliana phyllosphere communities. MBio 5:e00682–e00613

    Article  PubMed  PubMed Central  Google Scholar 

  • Markowitz V, Chen I, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova N, Kyrpides N (2012) IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 40:D115–D122. https://doi.org/10.1093/nar/gkr1044

    Article  CAS  PubMed  Google Scholar 

  • McMurdie PJ, Holmes S (2013) phyloseq : an R package for reproductible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4):e61217

  • Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider J, Piceno Y, DeSantis T, Andersen G, Bakker P, Raaijmakers J (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. https://doi.org/10.1126/science.1203980

    Article  CAS  PubMed  Google Scholar 

  • Mitter B, Pfaffenbichler N, Flavell R, Compant S, Antonielli L, Petric A, Berninger T, Naveed M, Sheibani-Tezerji R, von Maltzahn G, Sessitch A (2017) A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front Microbiol 8:11

    PubMed  PubMed Central  Google Scholar 

  • Munkvold GP (2009) Seed pathology progress in academia and industry. Annu Rev Phytopathol 47:285–311

    Article  CAS  PubMed  Google Scholar 

  • Nelson E (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309. https://doi.org/10.1146/annurev.phyto.42.121603.131041

    Article  CAS  PubMed  Google Scholar 

  • Nemergut D, Schmidt S, Fukami T, O'Neill S, Bilinski T, Stanish L, Knelman J, Darcy J, Lynch R, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356. https://doi.org/10.1128/MMBR.00051-12

    Article  PubMed  PubMed Central  Google Scholar 

  • Norros V, Penttilä R, Suominen M, Ovaskainen O (2012) Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales. Oikos 121:961–974

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, O’Hara MPR, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan : community ecology package. Ordination methods, diversity analysis and other function for community and vegetation ecologists. R package version 2.4–2. https://CRAN.R-project.org/package=vegan)

  • Panke-Buisse K, Poole A, Goodrich J, Ley R, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9:980–989. https://doi.org/10.1038/ismej.2014.196

    Article  CAS  PubMed  Google Scholar 

  • Paredes SH, Lebeis SL (2016) Giving back to the community: microbial mechanisms of plant-soil interactions. Funct Ecol 30:1043–1052

    Article  Google Scholar 

  • Peay K, Kennedy P, Talbot J (2016) Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14:434–447. https://doi.org/10.1038/nrmicro.2016.59

    Article  CAS  PubMed  Google Scholar 

  • Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110:6548–6553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rezki S, Campion C, Iacomi-Vasilescu B, Preveaux A, Toualbia Y, Bonneau S, Briand M, Laurent E, Hunault G, Simoneau P, Jacques M, Barret M (2016) Differences in stability of seed-associated microbial assemblages in response to invasion by phytopathogenic microorganisms. PeerJ 4:e1923. https://doi.org/10.7717/peerj.1923

  • Ritpitakphong U, Falquet L, Vimoltust A, Berger A, Metraux J, L'Haridon F (2016) The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol 210:1033–1043. https://doi.org/10.1111/nph.13808

    Article  CAS  PubMed  Google Scholar 

  • Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Cei FP, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331

    Article  PubMed  Google Scholar 

  • Santhanam R, Luu V, Weinhold A, Goldberg J, Oh Y, Baldwin I (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci U S A 112:E5013–E5020. https://doi.org/10.1073/pnas.1505765112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E, Lesniewski R, Oakley B, Parks D, Robinson C, Sahl J, Stres B, Thallinger G, Van Horn D, Weber C (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14:4–12

    Article  CAS  PubMed  Google Scholar 

  • Shade A, Jacques M-A, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol 37:15–22

    Article  PubMed  Google Scholar 

  • Sloan WT, Woodcock S, Lunn M, Head IM, Curtis TP (2007) Modeling taxa-abundance distributions in microbial communities using environmental sequence data. Microb Ecol 53:443–455

    Article  PubMed  Google Scholar 

  • Sommeria-Klein G, Zinger L, Taberlet P, Coissac E, Chave J (2016) Inferring neutral biodiversity parameters using environmental DNA data sets. Sci Rep 6:35644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama A, Bakker M, Badri D, Manter D, Vivanco J (2013) Relationships between Arabidopsis genotype-specific biomass accumulation and associated soil microbial communities. Botany-Botanique 91:123–126. https://doi.org/10.1139/cjb-2012-0217.

    Article  CAS  Google Scholar 

  • Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50. https://doi.org/10.1111/1758-2229.12181

    Article  Google Scholar 

  • Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K, Kyrpides NC, Pati A (2015) Microbial species delineation using whole genome sequences. Nucleic Acids Res 43:6761–6771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner M, Lundberg D, Coleman-Derr D, Tringe S, Dangl J, Mitchell-Olds T (2014) Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol Lett 17:717–726. https://doi.org/10.1111/ele.12276

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner M, Lundberg D, del Rio T, Tringe S, Dangl J, Mitchell-Olds T (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Garrity G, Tiedje J, Cole J (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woudenberg JHC, Groenewald JZ, Binder M, Crous PW (2013) Alternaria redefined. Stud Mycol 75:171–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by grant awarded by the Region des Pays de la Loire (metaSEED, 2013 10080) and the Michigan State University Plant Resilience Institute. The authors wish to thanks Gloria Torres-Cortes for manuscript assessment, Emmanuelle Laurent, Julie Gombert and Vincent Odeau (Fédération Nationale des Agriculteurs Multiplicateurs de Semences - FNAMS) for their help with all the field experiments, Aude Rochefort for the preparation of the sequencing library and Muriel Bahut from the platform ANAN of SFR Quasav for launching the MiSeq runs.

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Authors and Affiliations

  1. IRHS, INRA, AGROCAMPUS-Ouest, Université d’Angers, SFR4207 QUASAV, 42, rue Georges Morel, 49071, Beaucouzé, France

    Samir Rezki & Claire Campion

  2. INRA, UMR1345 Institut de Recherches en Horticulture et Semences, SFR4207 QUASAV, 42 rue Georges Morel, 49071, Beaucouzé, France

    Philippe Simoneau

  3. UMR1345 Institut de Recherches en Horticulture et Semences, Université d’Angers, 49071, Beaucouzé, France

    Marie-Agnès Jacques & Matthieu Barret

  4. Department of Microbiology and Molecular Genetics; Program in Ecology, Evolutionary Biology, and Behavior; The DOE Great Lakes Bioenergy Research Center; and The Plant Resilience Institute, Michigan State University, East Lansing, MI, 48824, USA

    Ashley Shade

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  1. Samir Rezki
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  2. Claire Campion
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  3. Philippe Simoneau
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Correspondence to Matthieu Barret.

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Rezki, S., Campion, C., Simoneau, P. et al. Assembly of seed-associated microbial communities within and across successive plant generations. Plant Soil 422, 67–79 (2018). https://doi.org/10.1007/s11104-017-3451-2

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