A microorganisms' journey between plant generations.

Nathan Vannier, Cendrine Mony, Anne-Kristel Bittebiere, Sophie Michon-Coudouel, Marine Biget, Philippe Vandenkoornhuyse
Author Information
  1. Nathan Vannier: Université de Rennes 1, CNRS, UMR 6553 EcoBio, campus Beaulieu, Avenue du Général Leclerc, 35042, Rennes Cedex, France. nathan.vannier35@gmail.com. ORCID
  2. Cendrine Mony: Université de Rennes 1, CNRS, UMR 6553 EcoBio, campus Beaulieu, Avenue du Général Leclerc, 35042, Rennes Cedex, France.
  3. Anne-Kristel Bittebiere: Université de Lyon 1, CNRS, UMR 5023 LEHNA, 43 Boulevard du 11 Novembre 1918, 69622, Villeurbanne Cedex, France.
  4. Sophie Michon-Coudouel: Université de Rennes 1, CNRS, UMS3343 OSUR, campus Beaulieu, Avenue du Général Leclerc, 35042, Rennes Cedex, France.
  5. Marine Biget: Université de Rennes 1, CNRS, UMS3343 OSUR, campus Beaulieu, Avenue du Général Leclerc, 35042, Rennes Cedex, France.
  6. Philippe Vandenkoornhuyse: Université de Rennes 1, CNRS, UMR 6553 EcoBio, campus Beaulieu, Avenue du Général Leclerc, 35042, Rennes Cedex, France.

Abstract

BACKGROUND: Plants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host. This microbiota can thus be considered a toolbox enabling plants to buffer local environmental changes, with a positive influence on plant fitness. In this context, the transmission of the microbiota to the progeny represent a way to ensure the presence of beneficial symbionts within the habitat. Examples of such transmission have been mainly described for seed transmission and concern a few pathogenic microorganisms. We investigated the transmission of symbiotic partners to plant progeny within clonal plant network.
METHODS: We used the clonal plant Glechoma hederacea as plant model and forced newly emitted clonal progeny to root in separated pots while controlling the presence of microorganisms. We used an amplicon sequencing approach of 16S and 18S rRNA targeting bacteria/archaea and fungi respectively to describe the root microbiota of mother and clonal-plant offspring.
RESULTS: We demonstrated the vertical transmission of a significant proportion of the mother plants' symbiotic bacteria and fungi to the daughters. Interestingly, archaea were not transmitted to the daughter plants. Transmitted communities had lower richness, suggesting a filtration during transmission. We found that the transmitted pool of microorganisms was similar among daughters, constituting the heritability of a specific cohort of microorganisms, opening a new understanding of the plant holobiont. We also found significant effects of distance to the mother plant and of growth time on the richness of the microbiota transmitted.
CONCLUSIONS: In this clonal plant, microorganisms are transmitted between individuals through connections, thereby ensuring the availability of microbe partners for the newborn plants as well as the dispersion between hosts for the microorganisms. This previously undescribed ecological process allows the dispersal of microorganisms in space and across plant generations. As the vast majority of plants are clonal, this process might be therefore a strong driver of ecosystem functioning and assembly of plant and microorganism communities in a wide range of ecosystems.

Keywords

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Grants

  1. EC2CO program (MIME project)/Centre National de la Recherche Scientifique
  2. PEPS program (MYCOLAND project)/Centre National de la Recherche Scientifique

MeSH Term

Archaea
Bacteria
Fungi
Lamiaceae
Microbiota
RNA, Ribosomal, 16S
RNA, Ribosomal, 18S
Soil Microbiology
Symbiosis

Chemicals

RNA, Ribosomal, 16S
RNA, Ribosomal, 18S

Word Cloud

Created with Highcharts 10.0.0plantmicroorganismstransmissionmicrobiotaplantsclonaltransmittedprogenymotherpresencewithinsymbioticpartnersusedrootfungisignificantdaughterscommunitiesrichnessfoundprocessdispersalgenerationsBACKGROUND:PlantscolonizedgreatdiversityformperformadditionalfunctionshostcanthusconsideredtoolboxenablingbufferlocalenvironmentalchangespositiveinfluencefitnesscontextrepresentwayensurebeneficialsymbiontshabitatExamplesmainlydescribedseedconcernpathogenicinvestigatednetworkMETHODS:Glechomahederaceamodelforcednewlyemittedseparatedpotscontrollingampliconsequencingapproach16S18SrRNAtargetingbacteria/archaearespectivelydescribeclonal-plantoffspringRESULTS:demonstratedverticalproportionplants'bacteriaInterestinglyarchaeadaughterTransmittedlowersuggestingfiltrationpoolsimilaramongconstitutingheritabilityspecificcohortopeningnewunderstandingholobiontalsoeffectsdistancegrowthtimeCONCLUSIONS:individualsconnectionstherebyensuringavailabilitymicrobenewbornwelldispersionhostspreviouslyundescribedecologicalallowsspaceacrossvastmajoritymightthereforestrongdriverecosystemfunctioningassemblymicroorganismwiderangeecosystemsmicroorganisms'journey16S/18SrRNAClonalMicrobiotaMicroorganismsVertical

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