The root‐invading pathogen Fusarium oxysporum targets pattern‐triggered immunity using both cytoplasmic and apoplastic effectors

Abstract

Plant pathogens use effector proteins to promote host colonisation. The mode of action of effectors from root-invading pathogens, such as Fusarium oxysporum (Fo), is poorly understood. Here, we investigated whether Fo effectors suppress pattern-triggered immunity (PTI), and whether they enter host cells during infection. Eight candidate effectors of an Arabidopsis-infecting Fo strain were expressed with and without signal peptide for secretion in Nicotiana benthamiana and their effect on flg22-triggered and chitin-triggered reactive oxidative species (ROS) burst was monitored. To detect uptake, effector biotinylation by an intracellular Arabidopsis-produced biotin ligase was examined following root infection. Four effectors suppressed PTI signalling; two acted intracellularly and two apoplastically. Heterologous expression of a PTI-suppressing effector in Arabidopsis enhanced bacterial susceptibility. Consistent with an intracellular activity, host cell uptake of five effectors, but not of the apoplastically acting ones, was detected in Fo-infected Arabidopsis roots. Multiple Fo effectors targeted PTI signalling, uncovering a surprising overlap in infection strategies between foliar and root pathogens. Extracellular targeting of flg22 signalling by a microbial effector provides a new mechanism on how plant pathogens manipulate their host. Effector translocation appears independent of protein size, charge, presence of conserved motifs or the promoter driving its expression.

A bacterial endophyte exploits chemotropism of a fungal pathogen for plant colonization

“…Invasive growth on the plant requires the functionally distinct Invasive Growth (IG) MAPK cascade [7][8][9][10] . Inside the plant, F. oxysporum secretes an array of effector proteins, which promote host colonization 11 . Among these, a functional homolog of the plant regulatory peptide RALF (rapid alkalinization factor) efficiently induces host alkalinization, which in turn stimulates MAPK-driven invasive growth 12,13 .…”

UhAVR1, an HR-triggering avirulence effector ofUstilago hordei, is secreted via the ER-Golgi pathway to the cytosol of barley coleoptile cells and contributes to virulence early in infection

“…The nonhost reaction in barley was also suppressed upon the delivery of UhAVR1+SP by the Psa T3SS ( Figure 4F-G) suggesting possible secretion followed by the re-entry of UhAVR1 in the host cytosol to suppress PTI. Very recently, several effectors from Arabidopsisinfecting Fusarium oxysporum have been shown to target PTI signalling upon re-entry into Nb cells [79]. Similarly, the delivery of UhAVR1+SP using the FoMV VOX vector produced necrosis in barley and in Nb (Figure 4C-E).…”

UhAVR1, an HR-Triggering Avirulence Effector of Ustilago hordei, Is Secreted via the ER–Golgi Pathway, Localizes to the Cytosol of Barley Cells during in Planta-Expression, and Contributes to Virulence Early in Infection

“…The nonhost reaction in barley was also suppressed upon the delivery of UhAVR1+SP by the Psa T3SS ( Figure 4 F–G) suggesting possible secretion followed by the re-entry of UhAVR1 in the host cytosol to suppress PTI. Very recently, several effectors from Arabidopsis -infecting Fusarium oxysporum have been shown to target PTI signalling upon re-entry into N. benthamiana cells [ 81 ]. Similarly, the delivery of UhAVR1+SP using the FoMV VOX vector produced necrosis in barley and in N. benthamiana ( Figure 4 C–E).…”