Secreted fungal effector lipase releases free fatty acids to inhibit innate immunity-related callose formation during wheat head infection.

Antje Blümke,Cornelia Herrfurth,Rainer Bode,Ivo Feussner,Björn Sode,Christian Falter,Wilhelm Schäfer,Christian A Voigt

doi:10.1104/pp.114.236737

Abstract

The deposition of the (1,3)-β-glucan cell wall polymer callose at sites of attempted penetration is a common plant defense response to intruding pathogens and part of the plant's innate immunity. Infection of the Fusarium graminearum disruption mutant Δfgl1, which lacks the effector lipase FGL1, is restricted to inoculated wheat (Triticum aestivum) spikelets, whereas the wild-type strain colonized the whole wheat spike. Our studies here were aimed at analyzing the role of FGL1 in establishing full F. graminearum virulence. Confocal laser-scanning microscopy revealed that the Δfgl1 mutant strongly induced the deposition of spot-like callose patches in vascular bundles of directly inoculated spikelets, while these callose deposits were not observed in infections by the wild type. Elevated concentrations of the polyunsaturated free fatty acids (FFAs) linoleic and α-linolenic acid, which we detected in F. graminearum wild type-infected wheat spike tissue compared with Δfgl1-infected tissue, provided clear evidence for a suggested function of FGL1 in suppressing callose biosynthesis. These FFAs not only inhibited plant callose biosynthesis in vitro and in planta but also partially restored virulence to the Δfgl1 mutant when applied during infection of wheat spikelets. Additional FFA analysis confirmed that the purified effector lipase FGL1 was sufficient to release linoleic and α-linolenic acids from wheat spike tissue. We concluded that these two FFAs have a major function in the suppression of the innate immunity-related callose biosynthesis and, hence, the progress of F. graminearum wheat infection.

Highlights

The deposition of the (1,3)-b-glucan cell wall polymer callose at sites of attempted penetration is a common plant defense response to intruding pathogens and part of the plant’s innate immunity
At 7 dpi, the strongest colonization of the spikelet’s transition zone occurred during F. graminearum wild type infection, and Dfgl1-2 revealed a relatively strong colonization compared with the nonadapted fungal pathogen P. teres (Fig. 1A)
Because we observed a strong repression of pathogeninduced, vascular callose deposition during F. graminearum wild type infection but not during Dfgl1-2 infection, we proposed that the secreted fungal lipase FGL1 could be involved in the inhibition of callose biosynthesis

Summary

Introduction

The deposition of the (1,3)-b-glucan cell wall polymer callose at sites of attempted penetration is a common plant defense response to intruding pathogens and part of the plant’s innate immunity. Elevated concentrations of the polyunsaturated free fatty acids (FFAs) linoleic and a-linolenic acid, which we detected in F. graminearum wild type-infected wheat spike tissue compared with Dfgl1-infected tissue, provided clear evidence for a suggested function of FGL1 in suppressing callose biosynthesis These FFAs inhibited plant callose biosynthesis in vitro and in planta and partially restored virulence to the Dfgl mutant when applied during infection of wheat spikelets. Further elucidation of the mechanisms of spreading resistance could support the generation of FHB-resistant wheat cultivars In this regard, we demonstrated that the secreted lipase FGL1 of F. graminearum is a virulence factor required for wheat infection (Voigt et al, 2005). Because the expression of the lipase-encoding gene LIP1 was induced in the biotrophic fungus Blumeria graminis during early stages of infection (Feng et al, 2009) and disruption of the putative secreted lipase gene lipA resulted in reduced virulence of the bacterial plant pathogen Xanthomonas campestris

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