Abstract
Phytophthora comprises a group of filamentous plant pathogens that cause serious crop diseases worldwide. It is widely known that a complex effector repertoire was secreted by Phytophthora pathogens to manipulate plant immunity and determine resistance and susceptibility. It is also recognized that Phytophthora pathogens may inhabit natural niches within complex environmental microbes, including bacteria. However, how Phytophthora pathogens interact with their cohabited microbes remains poorly understood. Here, we present such an intriguing case by using Phytophthora–bacteria interaction as a working system. We found that under co-culture laboratory conditions, several Phytophthora pathogens appeared to block the contact of an ecologically relevant bacterium, including Pseudomonas fluorescence and a model bacterium, Escherichia coli. We further observed that Phytophthora sojae utilizes a conserved Crinkler (CRN) effector protein, PsCRN63, to impair bacterial growth. Phytophthora capsici deploys another CRN effector, PcCRN173, to interfere with bacterial flagellum- and/or type IV pilus-mediated motility whereas a P. capsici-derived RxLR effector, PcAvh540, inhibits bacterial swimming motility, but not twitching motility and biofilm formation, suggesting functional diversification of effector-mediated Phytophthora–bacteria interactions. Thus, our studies provide a first case showing that the filamentous Phytophthora pathogens could deploy effectors to interfere with bacterial growth and motility, revealing an unprecedented effector-mediated inter-kingdom interaction between Phytophthora pathogens and bacterial species and thereby uncovering ecological significance of effector proteins in filamentous plant pathogens besides their canonical roles involving pathogen–plant interaction.
Highlights
Phytophthora spp., a genus of soilborne phytopathogenic oomycetes, infects a wide range of plants and crops to threaten crop production and cause devastating damage to the ecosystem globally (Kamoun et al, 2015)
We further found that P. sojae, a causal pathogen of soybean root and stem rot, could utilize a conserved CRN effector protein to interfere with bacterial growth, which acts as a mechanism explaining how Phytophthora pathogens block the contact of bacterial cells
To mimic a natural interaction between plant Phytophthora pathogens and ecologically relevant bacteria in the laboratory, we selected three representative plant Phytophthora pathogens (P. sojae, P. capsici, and P. nicotianae) to perform a coculture assay with a niche-associated widespread bacterial species, P. fluorescence
Summary
Phytophthora spp., a genus of soilborne phytopathogenic oomycetes, infects a wide range of plants and crops to threaten crop production and cause devastating damage to the ecosystem globally (Kamoun et al, 2015). Recent studies revealed that Phytophthora pathogens utilize effector proteins to manipulate plant immunity and promote infection (Dou and Zhou, 2012; Lamour et al, 2012; He et al, 2020). The P. infestans RxLR effector Pi06280 interacts with host susceptibility factor NRL1 to enhance the association between NRL1 and SWAP70, a guanine nucleotide exchange factor, by which Pi06280 promotes the proteasome-mediated degradation of SWAP70, leading to the suppression of plant immunity (He et al, 2018). In P. capsici, an RxLR effector, Avh103, targets host EDS1 and suppresses plant immunity, probably through promoting the disassociation of the EDS1–PAD4 complex (Li et al, 2020). The functionality of most effector proteins in Phytophthora still remains to be uncovered
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