Spatiotemporal nature of Fusarium graminearum-wheat coleoptile interactions

Abstract

Fusarium head blight (FHB) caused by the ascomycete fungus Fusarium graminearum can result in significant crop losses and render the crops harmful to human health due to contamination with mycotoxin. Although the pathogenesis of F. graminearum is widely investigated by molecular genetics approaches, detailed studies about its cellular and developmental processes at the initial stages of infection are very limited. We applied live-cell imaging approach to characterize the spatial and temporal development of growing hyphae and plant responses during F. graminearum and wheat coleoptile interactions. The present investigation demonstrates that F. graminearum uses two strategies to penetrate the host epidermal cells. The pathogen breaks through the host cell wall with appressoria-like structures derived from surficial hyphae, and also with the narrow pegs from thick and bulbous intracellular hyphae. Live cell imaging in the presence of the endocytic tracker FM4-64 showed that the plasma and intermembranes of the invaded wheat coleoptile cells were intact. Invasive hyphae exhibit branching, budding, pseudohyphae-like growth, cell-to-cell spreading ability, and were sealed within a plant membrane, indicating a biotrophic lifestyle of this fungus inside the invaded cells. Time-lapse imaging suggested that there were callose depositions at the plant cell walls in the form of continuous lines and also on the outer linings of the fungal invasive hyphae at colonization stage. In addition, our studies demonstrate that the activation of the toxisomerelated gene (TRI4) requires external stimuli and is spatio-temporally modulated. Generally, this study provides new insights into the colonization strategies and host response features during F. graminearum-plant interactions. Further tracing of cellular details will significantly contribute to our understanding of molecular mechanisms of F. graminearum-host interactions.

FgSpa2 recruits FgMsb3, a Rab8 GAP, to the polarisome to regulate polarized trafficking, growth and pathogenicity in Fusarium graminearum

“…The fungus infects its hosts through vulnerable openings or the stomata (Bushnell et al ., 2003). In addition, this fungus may form lobate appressoria and infection cushions during infection (Boenisch & Schäfer, 2011; Jiang et al ., 2019), and then colonize the host cells through hyphal elongation and apical growth (Jia et al ., 2019; Qiu et al ., 2019). During head blight infection, F. graminearum produces mycotoxins such as deoxynivalenol (DON) and zearalenone in cereal grains, which further threatens human and animal health (Cortinovis et al ., 2013).…”

Nicotinamide Mononucleotide Potentiates Resistance to Biotrophic Invasion of Fungal Pathogens in Barley

“…The results show that the number of appressoria-like structures was significantly reduced by NMN treatment at 24 hpi ( Figure 4 b). Appressoria-like structures are also observed in wheat as early infection structures that adhere tightly to the surface of coleoptile epidermal cells [ 17 ]. Similarly, the structures are also formed during penetration of neighboring epicarp cells from hyphae within the invaded cells [ 19 ].…”

“…However, observation with an optical microscope is limited by the fluorescence of the chlorenchyma of the spikelets, which obscures the morphology of the multilayered hyphae. Therefore, further detailed analysis of Stage I and Stage II was performed by confocal fluorescence microscopy using an F. graminearum strain expressing GFP constitutively and the epidermis of wheat coleoptiles, which are more easily observed due to its single-cell layer [ 17 ]. The coleoptile epidermal cells have been used as a suitable material to observe the morphogenesis of Bgh , which occurs relatively synchronously on time [ 18 ].…”

“…Since the host cells are still alive at this time, the lifestyle of F. graminearum is considered to be biotrophic. As the infection stage progresses further, it shifts to Stage II, which is necrotrophic [ 17 ].…”

Genome-Wide Identification and Characterization of Fusarium graminearum-Responsive lncRNAs in Triticum aestivum

“…Interestingly, we found that a large number of these DE lncRNAs (over 4130) were specifically expressed at 12 hpi, but only a few (89) were specifically expressed at 24 hpi, indicating the initial stage was the crucial stage for lncRNA-mediated gene regulation of wheat defense against F. graminearum . Recent research has shown F. graminearum initially colonizes the surface of the wheat coleoptile without immediate penetration, but intercellular space colonization happens at 5–8 h postinoculation [ 60 , 61 ]. Combining these recent results, an initial interaction between wheat and Fusarium was proposed.…”