Research Article: Non-canonical fungal G-protein coupled receptors promote Fusarium head blight on wheat

Date Published: April 1, 2019

Publisher: Public Library of Science

Author(s): Tess Dilks, Kirstie Halsey, Rebecca P. De Vos, Kim E. Hammond-Kosack, Neil Andrew Brown, Hui-Shan Guo.

http://doi.org/10.1371/journal.ppat.1007666

Abstract

Fusarium Head Blight (FHB) is the number one floral disease of cereals and poses a serious health hazard by contaminating grain with the harmful mycotoxin deoxynivalenol (DON). Fungi adapt to fluctuations in their environment, coordinating development and metabolism accordingly. G-protein coupled receptors (GPCRs) communicate changes in the environment to intracellular G-proteins that direct the appropriate biological response, suggesting that fungal GPCR signalling may be key to virulence. Here we describe the expansion of non-classical GPCRs in the FHB causing pathogen, Fusarium graminearum, and show that class X receptors are highly expressed during wheat infection. We identify class X receptors that are required for FHB disease on wheat, and show that the absence of a GPCR can cause an enhanced host response that restricts the progression of infection. Specific receptor sub-domains are required for virulence. These non-classical receptors physically interact with intracellular G-proteins and are therefore bona fide GPCRs. Disrupting a class X receptor is shown to dysregulate the transcriptional coordination of virulence traits during infection. This amounts to enhanced wheat defensive responses, including chitinase and plant cell wall biosynthesis, resulting in apoplastic and vascular occlusions that impede infection. Our results show that GPCR signalling is important to FHB disease establishment.

Partial Text

Wheat is prone to FHB disease when warm moist weather coincides with Fusarium graminearum spores arriving during crop anthesis. Germinating fungal spores produce hyphae that invade the inner surface of the floral tissues, with or without the production of complex infection structures [1]. The trichothecene (TRI) genes responsible for deoxynivalenol (DON) biosynthesis are highly expressed within these infection structures [1]. Once within the plant, invasive hyphae grow throughout the wheat head. Infection first spreads via symptomless colonisation of the apoplast, between live plant cells [2], during which the TRI genes are again highly expressed [3,4]. After the establishment of infection, the pathogen promotes the colonisation and deconstruction of dead plant cells, causing the visible bleached appearance characteristic of FHB disease [2]. DON is required for the establishment and progression of wheat infection. In DON’s absence, wheat cells mounts a defensive response that confines infection [5]. Other biologically active secreted molecules contribute to virulence [6], including the Fgl1 lipase that inhibits callose deposition and facilitates vasculature colonisation [7,8], the iron scavenging triacetyl fusarinine C siderophore [9–11], and carbohydrate-active enzymes that deconstruct plant cell walls and induce host cell death [2,4,12–15]. These virulence traits are spatially and temporally coordinated during infection [4], suggesting that the pathogen is responding to micro-environmental changes whilst inside the host.

The expansion of class X receptors in plant interacting Pezizomycota [27], and the identification of multiple class X receptors that contribute to FHB, reflects their function in pathogenesis. The first functionally characterised class X receptor, PTH11 in M. oryzae, senses hydrophobic plant surfaces, regulating appressoria development and host penetration [33]. FGRRES_16621-mediated signalling however, contributes to floral colonisation, but is not essential for host penetration. FGRRES_16621 is highly expressed at the advancing infection front, promoting the establishment of symptomless infection without activating host defences. Infection in the absence of FGRRES_16221 leads to rachis browning, elevated antifungal chitinases and plant polysaccharide biosynthetic gene expression, plus the appearance of apoplastic and vascular occlusions behind which intercellular hyphae accumulate. This shows the importance of the rachis to host defences and the outcome of F. graminearum infection.

 

Source:

http://doi.org/10.1371/journal.ppat.1007666

 

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