Abstract

Penetration resistance represents the first level of plant defense against phytopathogenic fungi. Here, we report that the starch-deficient Arabidopsis thaliana phosphoglucomutase (pgm) mutant has impaired penetration resistance against the hemibiotrophic fungus Colletotrichum higginsianum. We could not determine any changes in leaf cutin and epicuticular wax composition or indolic glucosinolate levels, but detected complex alterations in the cell wall monosaccharide composition of pgm. Notably, other mutants deficient in starch biosynthesis (adg1) or mobilization (sex1) had similarly affected cell wall composition and penetration resistance. Glycome profiling analysis showed that both overall cell wall polysaccharide extractability and relative extractability of specific pectin and xylan epitopes were affected in pgm, suggesting extensive structural changes in pgm cell walls. Screening of mutants with alterations in content or modification of specific cell wall monosaccharides indicated an important function of pectic polymers for penetration resistance and hyphal growth of C. higginsianum during the biotrophic interaction phase. While mutants with affected pectic rhamnogalacturonan-I (mur8) were hypersusceptible, penetration frequency and morphology of fungal hyphae were impaired on pmr5 pmr6 mutants with increased pectin levels. Our results reveal a strong impact of starch metabolism on cell wall composition and suggest a link between carbohydrate availability, cell wall pectin and penetration resistance.

Highlights

  • Penetration of the host leaf tissue by phytopathogenic degradation and physicomechanical force

  • In order to analyse the impact of reduced diurnal carbohydrate availability on the early biotrophic interaction phase between Arabidopsis and C. higginsianum, fungal development was examined in leaves of the starch-deficient phosphoglucomutase mutant

  • While the faster necrotrophic growth of C. higginsianum at 3 dpi can be explained by a reduction of induced defense responses in pgm leaves compared with wild type (Engelsdorf et al, 2013), we aimed at understanding the cause of increased fungal colonization in pgm between 1 and 2 dpi

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Summary

Introduction

Penetration of the host leaf tissue by phytopathogenic degradation and physicomechanical force. 702 | Engelsdorf et al. The plant cuticle and cell wall represent the first line of structural physicochemical barriers that oppose fungal penetration. The cuticle proper, containing the lipid polyester layer, cutin, is dominated by crosslinked hydroxylated C16 and C18 fatty acids with embedded intracuticular waxes. The cutin layer is covered by epicuticular wax crystals composed of very-long-chain (>C20) fatty acid derivatives (as reviewed by Beisson et al, 2012; Nawrath et al, 2013). Current models account an increased permeability of the cuticle to pathogen- or host-derived elicitors that are generated during cutin and cell wall degradation for a subsequently enhanced recognition by host cells (reviewed by Yeats and Rose, 2013). Contrasting correlations between cutin thickness and B. cinerea resistance have been obtained with other host plants

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