An oomycete effector subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface

Abstract

Eukaryotic cells deploy autophagy to eliminate invading microbes. In turn, pathogens have evolved effector proteins to counteract antimicrobial autophagy. How adapted pathogens co-opt autophagy for their own benefit is poorly understood. The Irish famine pathogen Phytophthora infestans secretes the effector protein PexRD54 that selectively activates an unknown plant autophagy pathway that antagonizes antimicrobial autophagy at the pathogen interface. Here, we show that PexRD54 induces autophagosome formation by bridging vesicles decorated by the small GTPase Rab8a with autophagic compartments labeled by the core autophagy protein ATG8CL. Rab8a is required for pathogen-triggered and starvation-induced but not antimicrobial autophagy, revealing specific trafficking pathways underpin selective autophagy. By subverting Rab8a-mediated vesicle trafficking, PexRD54 utilizes lipid droplets to facilitate biogenesis of autophagosomes diverted to pathogen feeding sites. Altogether, we show that PexRD54 mimics starvation-induced autophagy to subvert endomembrane trafficking at the host-pathogen interface, revealing how effectors bridge distinct host compartments to expedite colonization.

A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component

“…It is also possible that XopL is degraded by other additional mechanisms such as endocytosis or proteasome‐mediated degradation as it is most likely ubiquitinated by plant E3 ligases. In line with our observations on the autophagy pathway is that the ability of XopL to suppress the autophagy is still less than the recently discovered autophagy inhibitor AIMp (Pandey et al , 2021 ). This is also in line with the fact that loss of SH3P2 is only partially suppressing autophagy formation (Zhuang et al , 2013 ) while silencing of ATG7 or expression of AIMp result in a complete block of autophagy.…”

“…The induction of autophagosome formation and suppression of autophagic degradation prompted us to investigate host autophagy by immunoblotting for endogenous ATG8 and Joka2 in N. benthamiana (Svenning et al , 2011 ; Dagdas et al , 2016 ). We also used the previously described autophagy suppressor AIMp, a small peptide sequence derived from the Phytophthora PexRD54 effector (Pandey et al , 2021 ), as a positive control for autophagy suppression. The AIM peptide inhibits autophagosome biogenesis by occupying the binding pockets on ATG8 that mediate the docking of host autophagy adaptors such as Joka2 (Pandey et al , 2021 ).…”

“…We also used the previously described autophagy suppressor AIMp, a small peptide sequence derived from the Phytophthora PexRD54 effector (Pandey et al , 2021 ), as a positive control for autophagy suppression. The AIM peptide inhibits autophagosome biogenesis by occupying the binding pockets on ATG8 that mediate the docking of host autophagy adaptors such as Joka2 (Pandey et al , 2021 ). Joka2 protein abundance increased during infection, to a small extent 1‐day postinoculation (dpi), and to a greater extent at 2 dpi, while ATG8 protein levels only slightly increased at 2 dpi (Fig 1B ).…”

The complex roles of autophagy in plant immunity

“…This interaction allows the effector to be loaded into autophagosomes, eventually perturbing the interaction between ATG8CL and the autophagy cargo receptor Joka2 in tobacco, which is an NBR1 homolog. This ultimately confers defence against P. infestans infection [44,45].…”

Crossing paths: recent insights in the interplay between autophagy and intracellular trafficking in plants

“…Nevertheless, recent advances in understanding the interoperations of the autophagic pathway and these different post‐Golgi compartments in plants have been made [27]. Notable contributions to this understanding were recently achieved by identifying the involvement of the small GTPase Rab8a under oomycete infection conditions in Nicotiana benthamiana [28]. Rab GTPases comprise a large family of proteins involved in membrane trafficking between many different compartments [29,30].…”