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bioRxiv · 10.1101/2020.03.20.000117

The Irish potato famine pathogen subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface

Pandey, P.·Leary, A. Y.·Tümtas, Y.·Savage, Z.·Dagvadorj, B.·Tan, E.·Khandare, V.·Duggan, C.·Yusunov, T.·Madalinski, M.·Gabriel Mirkin, F.·Schornack, S.·Dagdas, Y.·Kamoun, S.·Bozkurt, T. O.
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Abstract

Eukaryotic cells deploy autophagy to eliminate invading microbes. In turn, pathogens have evolved effector proteins to counteract antimicrobial autophagy. How and why adapted pathogens co-opt autophagy for their own benefit is poorly understood. The Irish famine pathogen Phythophthora infestans secretes the effector protein PexRD54 that selectively activates an unknown plant autophagy pathway, while antagonizing antimicrobial autophagy. Here we show that PexRD54 induces autophagosome formation by bridging small GTPase Rab8a-decorated vesicles with autophagic compartments labelled by the core autophagy protein ATG8CL. Rab8a is required for pathogen-triggered and starvation-induced but not antimicrobial autophagy, revealing that specific trafficking pathways underpin selective autophagy. We discovered that Rab8a contributes to basal immunity against P. infestans, but PexRD54 diverts a sub-population of Rab8a vesicles to lipid droplets that associate with autophagosomes. These are then diverted towards pathogen feeding structures that are accommodated within the host cells. We propose that PexRD54 mimics starvation-induced autophagy by channeling host endomembrane trafficking towards the pathogen interface possibly to acquire nutrients. This work reveals that effectors can interconnect independent host compartments to stimulate complex cellular processes that benefit the pathogen. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/000117v1_ufig1.gif" ALT="Figure 1"> View larger version (83K): org.highwire.dtl.DTLVardef@bfc9fforg.highwire.dtl.DTLVardef@166b5f8org.highwire.dtl.DTLVardef@34d581org.highwire.dtl.DTLVardef@ad397f_HPS_FORMAT_FIGEXP M_FIG C_FIG

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Pandey, P., Leary, A. Y., Tümtas, Y., Savage, Z., Dagvadorj, B., Tan, E., Khandare, V., Duggan, C., Yusunov, T., Madalinski, M., Gabriel Mirkin, F., Schornack, S., Dagdas, Y., Kamoun, S., Bozkurt, T. O.. 2020-03-21. The Irish potato famine pathogen subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface. https://doi.org/10.1101/2020.03.20.000117

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