Abstract
Different phosphoinositides enriched at the membranes of specific subcellular compartments within plant cells contribute to organelle identity, ensuring appropriate cellular trafficking and function. During the infection of plant cells, biotrophic pathogens such as powdery mildews enter plant cells and differentiate into haustoria. Each haustorium is enveloped by an extrahaustorial membrane (EHM) derived from the host plasma membrane. Little is known about the EHM biogenesis and identity. Here, we demonstrate that among the two plasma membrane phosphoinositides in Arabidopsis (Arabidopsis thaliana), PI(4,5)P2 is dynamically up-regulated at powdery mildew infection sites and recruited to the EHM, whereas PI4P is absent in the EHM. Lateral transport of PI(4,5)P2 into the EHM occurs through a brefeldin A-insensitive but actin-dependent trafficking pathway. Furthermore, the lower levels of PI(4,5)P2 in pip5k1 pip5k2 mutants inhibit fungal pathogen development and cause disease resistance, independent of cell death-associated defenses and involving impaired host susceptibility. Our results reveal that plant biotrophic and hemibiotrophic pathogens modulate the subcellular distribution of host phosphoinositides and recruit PI(4,5)P2 as a susceptibility factor for plant disease.
Highlights
Filamentous phytopathogens have evolved numerous strategies to gain nutrients from host plants, but arguably one of the most specialized among these is that of the biotrophic fungi and oomycetes, which feed only on living plant cells to support their growth and propagation
By using genetically encoded biosensors for each phosphoinositide species in Arabidopsis thaliana challenged by the powdery mildew fungus Erysiphe cichoracearum, we show that among the two phosphoinositides at the plasma membrane (PM), PI(4,5)P2 pools were dynamically up107 regulated at pathogen infection sites and further integrated into the extrahaustorial membrane (EHM), whereas PI4P
We examined the subcellular localization of PI3P, PI4P and PI(4,5)P2 in leaves of transgenic Arabidopsis plants expressing mCITRINE-tagged variants of the biosensors mCIT-2xFYVEHRS, mCIT-2xPHFAPP1, and mCIT-1xPHPLCδ1, respectively (Simon et al, 2014), upon inoculation with the biotrophic powdery mildew fungus, Erysiphe cichoracearum (Ec)
Summary
Filamentous phytopathogens have evolved numerous strategies to gain nutrients from host plants, but arguably one of the most specialized among these is that of the biotrophic fungi and oomycetes, which feed only on living plant cells to support their growth and propagation. These pathogens consist of a diverse range of species from phylogenetically distinct groups: the fungal powdery mildews (Ascomycetes) and rusts (Basidiomycetes) and the oomycete downy mildews, cause substantial economic losses in major agricultural crops and environmental destruction in natural ecosystems. The biotrophic stage of hemibiotrophic fungi, without killing host cells, is a crucial step for the pathogen to initiate infection
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