1. UMR 1136, INRA-Nancy Université, Interactions Arbres/Microorganismes, INRA-Nancy, 54280 Champenoux, France
2. US DOE Joint Genome Institute, Walnut Creek, California 94598, USA
3. Microbial Ecology, Lund University, SE-223 62 Lund, Sweden
4. Architecture et Fonction des Macromolécules Biologiques, UMR 6098 CNRS-Universités Aix-Marseille I & II, 13288 Marseille Cedex 9, France
5. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Ghent, Belgium
6. Department of Biology, West Virginia University, Morgantown, West Virginia 26506, USA
7. Department for Plant Biochemistry, Georg-August-Universität Göttingen, 37077 Göttingen, Germany
8. Université Lyon 1, UMR CNRS - USC INRA d'Ecologie Microbienne, 69622 Villeurbanne, France
9. Stanford Human Genome Center, Department of Genetics, Stanford University School of Medicine, 975 California Avenue, Palo Alto, California 94304, USA
10. Institute of Forest Botany, Georg-August-Universität, 37077 Göttingen, Germany
11. Department of Biological Sciences, University of Alabama, Huntsville, Alabama 35899, USA
12. Eberhard-Karls-Universität, Physiologische Oekologie der Pflanzen, 72076 Tübingen, Germany
13. Department of Ecology & Evolution, University of Lausanne, 1015 Lausanne, Switzerland
14. Swiss Federal Research Institute WSL, 8903 Birmensdorf, Switzerland
15. Unité de Recherches en Génomique-Info, INRA-Evry, 91034 Évry Cedex, France
16. Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA
17. Department of Biology, The University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
18. Laboratoire Associé de l'INRA, Ghent University, B-9052 Gent, Belgium
19. Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102, USA

Correspondence to: F. Martin¹ Correspondence and requests for materials should be addressed to F.M. (Email: fmartin@nancy.inra.fr).

This article is distributed under the terms of the Creative Commons Attribution-Non-Commercial-Share Alike licence (http://creativecommons.org/licenses/by-nc-sa/3.0/), which permits distribution, and reproduction in any medium, provided the original author and source are credited. This licence does not permit commercial exploitation, and derivative works must be licensed under the same or similar licence.

Abstract

Mycorrhizal symbioses—the union of roots and soil fungi—are universal in terrestrial ecosystems and may have been fundamental to land colonization by plants^{1, 2}. Boreal, temperate and montane forests all depend on ectomycorrhizae¹. Identification of the primary factors that regulate symbiotic development and metabolic activity will therefore open the door to understanding the role of ectomycorrhizae in plant development and physiology, allowing the full ecological significance of this symbiosis to be explored. Here we report the genome sequence of the ectomycorrhizal basidiomycete Laccaria bicolor (Fig. 1) and highlight gene sets involved in rhizosphere colonization and symbiosis. This 65-megabase genome assembly contains 20,000 predicted protein-encoding genes and a very large number of transposons and repeated sequences. We detected unexpected genomic features, most notably a battery of effector-type small secreted proteins (SSPs) with unknown function, several of which are only expressed in symbiotic tissues. The most highly expressed SSP accumulates in the proliferating hyphae colonizing the host root. The ectomycorrhizae-specific SSPs probably have a decisive role in the establishment of the symbiosis. The unexpected observation that the genome of L. bicolor lacks carbohydrate-active enzymes involved in degradation of plant cell walls, but maintains the ability to degrade non-plant cell wall polysaccharides, reveals the dual saprotrophic and biotrophic lifestyle of the mycorrhizal fungus that enables it to grow within both soil and living plant roots. The predicted gene inventory of the L. bicolor genome, therefore, points to previously unknown mechanisms of symbiosis operating in biotrophic mycorrhizal fungi. The availability of this genome provides an unparalleled opportunity to develop a deeper understanding of the processes by which symbionts interact with plants within their ecosystem to perform vital functions in the carbon and nitrogen cycles that are fundamental to sustainable plant productivity.

Figure 1: Ectomycorrhizal symbiosis and the localization of the SSP MISSP7.

a, Fruiting bodies of L. bicolor colonizing seedlings of Douglas fir (photograph courtesy of D. Vairelles). b, Laser-scanning confocal microscopy image of a transverse section of Pseudotsuga menziesii–L. bicolor ectomycorrhizae showing extramatrical mycelium (em), the mantle (m) and Hartig net hyphae (hn) between epidermal (ec), tannin (tc) and cortical (cc) root cells. Scale, 10 m. c–f, Immunofluorescent localization of MISSP7. Transverse (c, e) and longitudinal (d, f) sections of P. trichocarpa–L. bicolor ectomycorrhizae. MISSP7 was detected in the hyphae of the mantle (m) and the Hartig net (hn) ensheathing epidermal cells (ec). Rectangles in d and f show the finger-like, labyrinthine hyphal system accumulating a large amount of MISSP7. e, f, Phase contrast images. Scale, 10 m.

High resolution image and legend (238K)

1. UMR 1136, INRA-Nancy Université, Interactions Arbres/Microorganismes, INRA-Nancy, 54280 Champenoux, France
2. US DOE Joint Genome Institute, Walnut Creek, California 94598, USA
3. Microbial Ecology, Lund University, SE-223 62 Lund, Sweden
4. Architecture et Fonction des Macromolécules Biologiques, UMR 6098 CNRS-Universités Aix-Marseille I & II, 13288 Marseille Cedex 9, France
5. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, B-9052 Ghent, Belgium
6. Department of Biology, West Virginia University, Morgantown, West Virginia 26506, USA
7. Department for Plant Biochemistry, Georg-August-Universität Göttingen, 37077 Göttingen, Germany
8. Université Lyon 1, UMR CNRS - USC INRA d'Ecologie Microbienne, 69622 Villeurbanne, France
9. Stanford Human Genome Center, Department of Genetics, Stanford University School of Medicine, 975 California Avenue, Palo Alto, California 94304, USA
10. Institute of Forest Botany, Georg-August-Universität, 37077 Göttingen, Germany
11. Department of Biological Sciences, University of Alabama, Huntsville, Alabama 35899, USA
12. Eberhard-Karls-Universität, Physiologische Oekologie der Pflanzen, 72076 Tübingen, Germany
13. Department of Ecology & Evolution, University of Lausanne, 1015 Lausanne, Switzerland
14. Swiss Federal Research Institute WSL, 8903 Birmensdorf, Switzerland
15. Unité de Recherches en Génomique-Info, INRA-Evry, 91034 Évry Cedex, France
16. Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA
17. Department of Biology, The University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
18. Laboratoire Associé de l'INRA, Ghent University, B-9052 Gent, Belgium
19. Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102, USA

Correspondence to: F. Martin¹ Correspondence and requests for materials should be addressed to F.M. (Email: fmartin@nancy.inra.fr).

This article is distributed under the terms of the Creative Commons Attribution-Non-Commercial-Share Alike licence (http://creativecommons.org/licenses/by-nc-sa/3.0/), which permits distribution, and reproduction in any medium, provided the original author and source are credited. This licence does not permit commercial exploitation, and derivative works must be licensed under the same or similar licence.

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