Modulation of plant autophagy during pathogen attack

Leary, Alexandre Y; Sanguankiattichai, Nattapong; Duggan, Cian; Tümtaş, Yasin; Pandey, Pooja; Segretin, María Eugenia; Salguero‐Linares, Jose; Savage, Zachary; Yow, Rui Jin; Bozkurt, Tolga O.

doi:10.1093/jxb/erx425

Cited by 55 publications

(56 citation statements)

References 73 publications

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“…Joka2/NBR1 is also required for immunity against bacteria and oomycete pathogens, however, the extent to which defense-related autophagy acts against these pathogens is unknown (Dagdas et al, 2018; Hofius et al, 2018). Consistent with the important role of autophagy in plant immunity, adapted pathogens appear to have evolved strategies to manipulate the host autophagy machinery to support their virulence (Hofius et al, 2018; Leary et al, 2017, 2019).…”

Section: Introductionmentioning

confidence: 99%

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

Pandey

Leary

Tümtaş

et al. 2020

Preprint

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Eukaryotic cells deploy autophagy to eliminate invading microbes. In turn, pathogens have evolved 22 effector proteins to counteract antimicrobial autophagy. How and why adapted pathogens co-opt 23 autophagy for their own benefit is poorly understood. The Irish famine pathogen Phythophthora 24 infestans secretes the effector protein PexRD54 that selectively activates an unknown plant 25 autophagy pathway, while antagonizing antimicrobial autophagy. Here we show that PexRD54 26 induces autophagosome formation by bridging small GTPase Rab8a-decorated vesicles with 27 autophagic compartments labelled by the core autophagy protein ATG8CL. Rab8a is required for 28 pathogen-triggered and starvation-induced but not antimicrobial autophagy, revealing that specific 29 trafficking pathways underpin selective autophagy. We discovered that Rab8a contributes to basal 30 immunity against P. infestans, but PexRD54 diverts a sub-population of Rab8a vesicles to lipid 31 droplets that associate with autophagosomes. These are then diverted towards pathogen feeding 32 structures that are accommodated within the host cells. We propose that PexRD54 mimics starvation-33 induced autophagy by channeling host endomembrane trafficking towards the pathogen interface 34 possibly to acquire nutrients. This work reveals that effectors can interconnect independent host 35 compartments to stimulate complex cellular processes that benefit the pathogen. Graphical abstract: 37 38 39 40 41 42 43 44 45 Introduction: 46 47Autophagy is a conserved eukaryotic cellular process that mediates the lysosomal degradation and 48 relocation of cellular cargoes within double-membraned vesicles called autophagosomes (He and 49 Klionsky, 2009; Leidal et al., 2020). Although autophagy is historically considered to be a bulk 50 catabolic pathway tasked with maintaining cellular homeostasis under normal or stress conditions, it 51 is now clear that autophagy can be highly selective in cargo choice (Zaffagnini and Martens, 2016). 52Autophagic cargoes are typically captured during autophagosome formation, a complex process that 53 is regulated by the concerted action of a set of conserved autophagy related proteins (ATG) as well 54 as specialized autophagy adaptors and cargo receptors (Mizushima et al., 2011). These captured 55 cargoes are sorted within the autophagosome during maturation of the isolation membrane (also 56 known as the phagophore) via the specific interactions between cargo receptors and a lipidated form 57 of ATG8, which decorates the phagophore to serve as a docking platform for cargo receptors 58 (Ryabovol and Minibayeva, 2016; Slobodkin and Elazar, 2013). 60The source of the phagophore is still under debate, but its primary source is considered to be the 61 endoplasmic reticulum (ER) (Bernard and Klionsky, 2013; Hamasaki et al., 2013). As the cargo is 62 being captured, the phagophore undergoes massive expansion and finally gets sealed to form a 63 mature autophagosome. Therefore, formation of the autophagosome requires additional lipid supplies 64...

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Section: Introductionmentioning

confidence: 99%

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

Pandey

Leary

Tümtaş

et al. 2020

Preprint

Self Cite

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“…Autophagy participates in the regulation of plant cell death, viral clearance, and antimicrobial defenses, but the underlying molecular mechanisms are poorly understood. Notably, pathogens seem to have evolved ways not only to evade autophagic clearance but also to manipulate and subvert autophagy for their own benefit (for further reading refer to [145,146]).…”

Section: Discussionmentioning

confidence: 99%

Plant Cells under Attack: Unconventional Endomembrane Trafficking during Plant Defense

Ruano

Scheuring

2020

Plants

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Since plants lack specialized immune cells, each cell has to defend itself independently against a plethora of different pathogens. Therefore, successful plant defense strongly relies on precise and efficient regulation of intracellular processes in every single cell. Smooth trafficking within the plant endomembrane is a prerequisite for a diverse set of immune responses. Pathogen recognition, signaling into the nucleus, cell wall enforcement, secretion of antimicrobial proteins and compounds, as well as generation of reactive oxygen species, all heavily depend on vesicle transport. In contrast, pathogens have developed a variety of different means to manipulate vesicle trafficking to prevent detection or to inhibit specific plant responses. Intriguingly, the plant endomembrane system exhibits remarkable plasticity upon pathogen attack. Unconventional trafficking pathways such as the formation of endoplasmic reticulum (ER) bodies or fusion of the vacuole with the plasma membrane are initiated and enforced as the counteraction. Here, we review the recent findings on unconventional and defense-induced trafficking pathways as the plant´s measures in response to pathogen attack. In addition, we describe the endomembrane system manipulations by different pathogens, with a focus on tethering and fusion events during vesicle trafficking.

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“…However, some evidence suggests that autophagy may also promote PCD in response to abiotic stress (Barany et al, 2018). This dual function of autophagy is better characterized in the plant’s innate immune system, where autophagy has been shown to act as either a survival or cell-death pathway, depending on the type of pathogen (i.e., biotrophic or necrotrophic) and the type of plant immune receptors involved in the response (Zhou et al, 2014; Leary et al, 2017; Üstün et al, 2017). Genetic analysis in Arabidopsis and tobaco plants has indicated a critical role for autophagy in the initiation and promotion of the HR upon infection with avirulent strains of different pathogens, including Pseudomonas syringae pv.…”

Section: Discussionmentioning

confidence: 99%

Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death

Teper‐Bamnolker

Danieli

Peled-Zehavi

et al. 2019

Preprint

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One sentence summary: Carbon starvation induced programmed cell death 26 by trafficking vacuolar processing enzyme through the autophagy pathway to 27 the vacuole. 28 29The author responsible for distribution of materials integral to the findings 30 presented in this article in accordance with the policy described in the 31 Instructions for Authors (www.plantcell.org) is: Dani Eshel (dani@agri.gov.il). 32 33 34 2 35 Abstract 36 37 The caspase-like vacuolar processing enzyme (VPE) is a key factor in 38 programmed cell death (PCD) associated with plant stress responses. Growth 39 medium lacking a carbon source and dark conditions caused punctate labeling 40 of 35S::VPE1-GFP (StVPE1-GFP) in potato leaves. Carbon starvation of BY-2 41 cells induced higher VPE activity and PCD symptoms. Growing VPE-RNAi BY-42 2 cells without sucrose reduced VPE activity and prevented PCD symptoms. 43 During extended exposure to carbon starvation, VPE expression and activity 44 levels peaked, with a gradual increase in BY-2 cell death. Histological analysis 45 of StVPE1-GFP in BY-2 cells showed that carbon starvation induces its 46 translocation from the endoplasmic reticulum to the central vacuole, through 47 tonoplast engulfment. Exposure of BY-2 culture to the autophagy inhibitor 48 concanamycin A caused autophagic bodies accumulation in the cell vacuole. 49 Such accumulation did not occur in the presence of 3-methyladenine, an 50 inhibitor of early-stage autophagy. BY-2 cells constitutively expressing 51 StATG8IL-RFP, an autophagosome marker, showed colocalization with the 52 StVPE1-GFP protein in the cytoplasm and vacuole. RNAi silencing of the core 53 autophagy component ATG4 in BY-2 cells reduced VPE activity and cell death. 54 These results are the first to suggest that VPE translocates to the cell vacuole 55 through the autophagy pathway, leading to PCD. 56 endopeptidase activity, unlike caspases that cleave their substrates at aspartic 91 acid residues (Silva et al., 2005; Van Durme and Nowack, 2016). The VPE 92 proteins belong to a family of cysteine proteinases that are well conserved 93 among a variety of organisms, including many plant and animal species (Cai 94 and Gallois, 2015; Hatsugai et al., 2015; Sueldo and van der Hoorn, 2017). 95 VPEs were originally found to be responsible for the maturation of seed 96 storage proteins and various other vacuolar proteins in plants (Hara-Nishimura 97 et al., 1991; Hara-Nishimura et al., 1993; Hatsugai et al., 2004). VPE, which is 98 released into the vacuole during PCD, triggers the degradation of other 99 proteins (Hara-Nishimura et al., 2005; Kuroyanagi et al., 2005; Van Durme and 100 Nowack, 2016). VPEs, which exhibit caspase-1-like activity, play important 101 roles in plant PCD, be it developmental or in response to biotic or abiotic stress 102 (reviewed by Hatsugai et al., 2015; Vorster et al., 2019). Specifically, VPE has 103 been characterized as a major factor in the HR. By silencing the gene 104 encoding VPE, Hatsugai et al. (2004) showed that vacuolar collapse, caused ...

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Modulation of plant autophagy during pathogen attack

Cited by 55 publications

References 73 publications

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

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

Plant Cells under Attack: Unconventional Endomembrane Trafficking during Plant Defense

Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death

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