Traffic Control: Subversion of Plant Membrane Trafficking by Pathogens

Abstract

Membrane trafficking pathways play a prominent role in plant immunity to parasitic organisms. Primarily, the endomembrane transport system coordinates membrane-bound cellular organelles to ensure that immunological components are utilized effectively during pathogen resistance. Adapted pathogens and pests have evolved to interfere with aspects of membrane transport systems to subvert host plant immunity. To do this, they secrete virulence factors known as effectors, many of which converge on host membrane trafficking routes. The emerging paradigm is that effectors redundantly target every step of membrane trafficking from vesicle budding to trafficking and membrane fusion. In this review, we focus on the mechanisms adopted by plant pathogens to reprogram host plant vesicle trafficking, providing examples of effector-targeted transport pathways and highlighting key questions for the field to answer moving forward. Expected final online publication date for the Annual Review of Phytopathology, Volume 61 is September 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

An RXLR effector targets ER-Golgi interface to induce ER stress and necrotic cell death

“…Numerous studies have reported that pathogenic effectors target vesicle-associated proteins to disrupt the secretion of defense-related proteins or to subvert autophagy to obtain nutrients for pathogen nutrition (Gu et al 2017; Pandey et al 2021; Petre et al 2021; Yuen et al 2023). In our research, we have shown that Pc12 targets Rab13-2 and disrupts vesicle trafficking between the ER and the Golgi.…”

An oomycete effector co-opts a host RabGAP protein to remodel pathogen interface and subvert defense-related secretion

“…Filamentous plant pathogens, including oomycetes and fungi, project hyphal extensions that breach the cell wall and penetrate host cells. At these junctures, plants mount targeted immune responses, which include cellular reinforcements and secretion of defense molecules [7][8][9][10] . Filamentous pathogens have developed strategies to overcome these defenses, forming specialized infection structures like haustoria or infection vesicles (formed by oomycete pathogens), which are accommodated inside host cells.…”

“…The critical role of membrane trafficking in plant pathogen defense is increasingly evident, with diverse pathogens deploying effectors that virtually target every facet of vesicle trafficking 5,6,10,[18][19][20] . Proteomic screens have highlighted the strategic targeting of the host vesicle trafficking system by Phytophthora pathogens 6,21 .…”

Logistics of defense: The contribution of endomembranes to plant innate immunity

“…Coevolution of plant–pathogen interactions has led plants to adopt multiple defense strategies exhibiting functional diversification and partial redundancy ( Upson et al, 2018 ; Derevnina et al, 2021 ). In turn, pathogens have evolved effectors aimed at avoiding detection, subverting immune pathways, and maintaining a virulent advantage ( Yuen et al, 2023 ; Jeon and Segonzac, 2023 ). We will take an inside-out view of a cell under pathogen attack, starting from the ER and ending in the extracellular space, and we will discuss how preformed organelles and mechanisms of defense are targeted by pathogens to dampen immunity, and how plants respond to this challenge.…”