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Metabolic processes and carbon nutrient exchanges between host and pathogen sustain the disease development during sunflower infection by Sclerotinia sclerotiorum

Planta volume 226, pages 251–265 (2007)Cite this article

Abstract

Interactions between the necrotrophic fungus Sclerotinia sclerotiorum and one of its hosts, Helianthus annuus L., were analyzed during fungal colonization of plant tissues. Metabolomic analysis, based on 13C- and 31P-NMR spectroscopy, was used to draw up the profiles of soluble metabolites of the two partners before interaction, and to trace the fate of metabolites specific of each partner during colonization. In sunflower cotyledons, the main soluble carbohydrates were glucose, fructose, sucrose and glutamate. In S. sclerotiorum extracts, glucose, trehalose and mannitol were the predominant soluble carbon stores. During infection, a decline in sugars and amino acids was observed in the plant and fungus total content. Sucrose and fructose, initially present almost exclusively in plant, were reduced by 85%. We used a biochemical approach to correlate the disappearance of sucrose with the expression and the activity of fungal invertase. The expression of two hexose transporters, Sshxt1 and Sshxt2, was enhanced during infection. A database search for hexose transporters homologues in the S. sclerotiorum genome revealed a multigenic sugar transport system. Furthermore, the composition of the pool of reserve sugars and polyols during infection was investigated. Whereas mannitol was produced in vitro and accumulated in planta, glycerol was exclusively produced in infected tissues and increased during colonization. The hypothesis that the induction of glycerol synthesis in S. sclerotiorum exerts a positive effect on osmotic protection of fungal cells and favors fungal growth in plant tissues is discussed. Taken together, our data revealed the importance of carbon–nutrient exchanges during the necrotrophic pathogenesis of S. sclerotiorum.

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Abbreviations

GPC:

Glycerylphosphoryl-choline

GPE:

Glycerylphosphoryl-ethanolamine

GPG:

Glycerylphosphoryl-glycerol

GPI:

Glycerylphosphoryl-inositol

hpi:

Hours post-inoculation

PCA:

Perchloric acid

PGA:

Phosphoglyceric acid

Q-PCR:

Quantitative polymerase chain reaction

UDP-GlcNAc:

Uridine-5′-diphosphate-N-acetylglucosamine

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Acknowledgments

This work was supported by grants from the Ministère de la recherche, CNRS, the Université de Lyon, and the Région Rhône-Alpes. CJ was supported by a doctoral scholarship from the Région Rhône-Alpes. We thank AJ Dorne and MH Lebrun (Plant and Fungal Physiology, UMR 2847 CNRS-BayerCropScience, Lyon, France) for helpful comments. We are also indebt to JL Lebail for his dedicated technical assistance with the NMR spectrometer.

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  1. Laboratoire de Pathogénie des Champignons Nécrotrophes, CNRS, UMR5122, Unité Microbiologie et Génétique, Université Lyon 1, Bat Lwoff, 10 rue Raphaël Dubois, Villeurbanne, 69622, France

    Cécile Jobic, Christine Rascle, Michel Fèvre & Pascale Cotton

  2. Laboratoire de Physiologie Cellulaire Végétale, Département Réponse et Dynamique Cellulaires, CEA-Grenoble, Université Joseph Fourier, UMR 5168, CEA, CNRS, INRA, 17 rue des Martyrs, Grenoble Cedex 9, 38054, France

    Anne-Marie Boisson, Elisabeth Gout & Richard Bligny

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  1. Cécile Jobic
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  2. Anne-Marie Boisson
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  3. Elisabeth Gout
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  4. Christine Rascle
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  5. Michel Fèvre
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Correspondence to Pascale Cotton.

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Jobic, C., Boisson, AM., Gout, E. et al. Metabolic processes and carbon nutrient exchanges between host and pathogen sustain the disease development during sunflower infection by Sclerotinia sclerotiorum . Planta 226, 251–265 (2007). https://doi.org/10.1007/s00425-006-0470-2

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  • DOI: https://doi.org/10.1007/s00425-006-0470-2

Keywords

  • Acid invertase
  • Helianthus
  • Hexose transport
  • NMR spectroscopy
  • Polyols
  • Sclerotinia