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Opinion/Hypothesis | Host-Microbe Biology

Clonal Plants as Meta-Holobionts

Nathan Vannier, Cendrine Mony, Anne-Kristel Bittebiere, Kevin R. Theis, Eugene Rosenberg, Philippe Vandenkoornhuyse
Michelle Heck, Editor
Nathan Vannier
aUniversité de Rennes, CNRS, UMR6553 EcoBio, Rennes, France
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Cendrine Mony
aUniversité de Rennes, CNRS, UMR6553 EcoBio, Rennes, France
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Anne-Kristel Bittebiere
bUniversité de Lyon 1, CNRS, Villeurbanne, France
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Kevin R. Theis
cDepartment of Biochemistry, Microbiology and Immunology, Wayne State University, Detroit, Michigan, USA
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Eugene Rosenberg
dDepartment of Molecular Microbiology and Biotechnology, Tel-Aviv University, Tel Aviv, Israel
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Philippe Vandenkoornhuyse
aUniversité de Rennes, CNRS, UMR6553 EcoBio, Rennes, France
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Michelle Heck
Cornell University
Roles: Editor
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DOI: 10.1128/mSystems.00213-18
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  • FIG 1
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    FIG 1

    Organization of a clonal plant, sequential growth, and plastic responses in heterogeneous environments. (Top left) Clonal fragments are composed of ramets linked through connections that can be aboveground or belowground (see supplemental material for vocabulary definitions). (Bottom left) Clonal growth is sequential and multiplies ramets and connections. A clonal fragment can be split due to physical injury or connection life span. (Right) Clonal fragments display particular plastic responses unique to clonal plants that are “foraging behavior” (a), “specialization for abundance” (b), and “division of labor” (c). Foraging behavior consists of aggregating the ramets in rich patches (brown) and avoiding poor patches (gray). Plastic responses may include connection length, direction of growth, and intensity of ramification. Specialization for abundance describes when ramets locally invest in organs that uptake the most abundant resource and share this resource to the other ramets thanks to physiological integration. Division of labor is an extension of specialization when the environment presents two resources that are negatively correlated (such as light and soil resources). Ramets thus display high aboveground allocation under high-light and low-nutrient conditions, whereas the belowground allocation is high under the reverse conditions.

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    FIG 2

    Meta-holobiont and importance of transmission between holobionts. (Top) The structure of the meta-holobiont is explained. Colored dots, triangles, and squares correspond to epiphytic or endophytic microorganisms forming the root microbiota. Note that all plant compartments (i.e., roots and shoots) are colonized by microorganisms even if not illustrated in this figure. Transmission can be vertical through seeds (1) or through connections (2) and pseudovertical (3). (Bottom) The relative importance of 2 and 3 depending on the clonal strategy in terms of architecture of the clonal network (phalanx versus guerrilla) (a) and life span of the connection (splitter versus integrator) (b).

  • FIG 3
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    FIG 3

    Links between meta-holobiont and meta-community. Clonal network comprises ramets connected by horizontal modified stems. Each ramet is under the influence of a local abiotic environment. Metacommunities are defined as a set of local communities linked by dispersal of multiple potentially interacting species (40). The figure presents the four main processes driving the assemblages at the metacommunity scale (local habitat patch conditions, patch disturbance, dispersal, and random processes) and the corresponding paradigms as defined by Leibold et al. (40). This is a simplified view of the metacommunity assembly rules, as all four processes interplay in each of the paradigms. Their transposition of the meta-holobiont scale is described on the right. Gray gradient indicates the habitat patch environmental conditions, and black arrows indicate the dispersal fluxes between a given habitat patch pair.

Supplemental Material

  • Figures
  • FIG S1

    Glechoma hederacea phenotypic plasticity induced by its microbiota composition. All the plants have the same genotype (i.e., they are from the same clone), are growing under controlled conditions (light, temperature, hygrometry, and water supply), and differ only in a single component of their microbiota (i.e., mycorrhizal colonizer). The picture shows a clone of G. hederacea that has been inoculated with an isolate of Rhizophagus invermaius, Glomus diaphanum, or Archaeospora trappei (R.in, G, or A, respectively). T is the nonmycorrhized control. Download FIG S1, TIF file, 1.3 MB.

    Copyright © 2019 Vannier et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TEXT S1

    Different scales of clonality and definitions. Download Text S1, DOC file, 0.02 MB.

    Copyright © 2019 Vannier et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Clonal Plants as Meta-Holobionts
Nathan Vannier, Cendrine Mony, Anne-Kristel Bittebiere, Kevin R. Theis, Eugene Rosenberg, Philippe Vandenkoornhuyse
mSystems Mar 2019, 4 (2) e00213-18; DOI: 10.1128/mSystems.00213-18

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Clonal Plants as Meta-Holobionts
Nathan Vannier, Cendrine Mony, Anne-Kristel Bittebiere, Kevin R. Theis, Eugene Rosenberg, Philippe Vandenkoornhuyse
mSystems Mar 2019, 4 (2) e00213-18; DOI: 10.1128/mSystems.00213-18
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  • Top
  • Article
    • ABSTRACT
    • OPINION/HYPOTHESIS
    • THE GENOME IS NOT THE ONLY GENETIC SOURCE OF PHENOTYPIC VARIATION AMONG MACROORGANISMS
    • HOLOBIONT AND HOLOGENOME CONCEPTS
    • HOLOBIONT MICROBIOTA ASSEMBLY
    • PLANT HOLOBIONTS AND HOLOGENOMES: A SPECIAL CASE
    • BEYOND HOLOBIONTS: CLONAL PLANTS AS META-HOLOBIONTS
    • THE META-HOLOBIONT CONCEPT
    • IMPACT OF MICROBIAL TRANSMISSION WITHIN THE META-HOLOBIONT
    • HOLOBIONT DYNAMICS WITHIN THE META-HOLOBIONT NETWORK: APPLICATION OF METACOMMUNITY-BASED THEORIES
    • NETWORK THEORY AND META-HOLOBIONT PROPERTIES
    • ACKNOWLEDGMENTS
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

holobiont
plant-microbe interactions
symbiosis

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