Abstract
Fusarium graminearum is one of the most destructive plant pathogens worldwide, causing fusarium head blight (FHB) on cereals. F. graminearum colonizes wheat plant surfaces with specialized unbranched hyphae called runner hyphae (RH), which develop multicelled complex appressoria called infection cushions (IC). IC generate multiple penetration sites, allowing the fungus to enter the plant cuticle. Complex infection structures are typical for several economically important plant pathogens, yet with unknown molecular basis. In this study, RH and IC formed on the surface of wheat paleae were isolated by laser capture microdissection. RNA‐Seq‐based transcriptomic analyses were performed on RH and IC and compared to mycelium grown in complete medium (MY). Both RH and IC displayed a high number of infection up‐regulated genes (982), encoding, among others, carbohydrate‐active enzymes (CAZymes: 140), putative effectors (PE: 88), or secondary metabolism gene clusters (SMC: 12 of 67 clusters). RH specifically up‐regulated one SMC corresponding to aurofusarin biosynthesis, a broad activity antibiotic. IC specifically up‐regulated 248 genes encoding mostly putative virulence factors such as 7 SMC, including the mycotoxin deoxynivalenol and the newly identified fusaoctaxin A, 33 PE, and 42 CAZymes. Furthermore, we studied selected candidate virulence factors using cellular biology and reverse genetics. Hence, our results demonstrate that IC accumulate an arsenal of proven and putative virulence factors to facilitate the invasion of epidermal cells.
Highlights
Fusarium head blight (FHB), caused by Fusarium graminearum, is a devastating disease of cereals including wheat, barley, oats, and rye with large economic impacts (Savary et al, 2012)
The large-scale reprogramming of appressorial gene expression of the plant pathogens M. oryzae and Colletotrichum species is well known (O’Connell et al, 2012; Soanes et al, 2012)
The transcriptomes of hyphae grown in culture (MY) and epiphytically grown runner hyphae (RH) revealed fundamental transcriptional differences
Summary
Fusarium head blight (FHB), caused by Fusarium graminearum, is a devastating disease of cereals including wheat, barley, oats, and rye with large economic impacts (Savary et al, 2012). To identify genes differentially expressed during infection, we extracted RNA from F. graminearum hyphae (MY) growing in CM. The highest transcriptional changes on infection regulated secreted proteins were on CAZymes, ROS, and PE (Table S4). The main gene families corresponding to infection up-regulated genes in IC were SMC (38 genes, corresponding to 16 clusters), CAZymes (42), ROS (34), and PE (33) (Table 3) This comparison shows that IC expressed a specific set of putative virulence factors (CAZymes, PE, and SMC), which we further investigated. To test whether aurofusarin could act as an antibiotic against microbial competitors growing on the wheat floral tissue's surface, the toxicity of aurofusarin on bacteria and fungi was assessed using mycelium extracts from either WT or the aurofusarindeficient Δpks mutant (Figure 8b and Table S12). Extracts from Δpks were completely nontoxic to all tested organisms, demonstrating that aurofusarin is responsible for the observed toxicity of WT extract to bacteria and fungi
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