An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor

Dagdas, Yasin; Belhaj, Khaoula; Maqbool, Abbas; Chaparro-Garcia, Angela; Pandey, Pooja; Pêtre, Benjamin; Tabassum, Nadra; Cruz-Mireles, Neftaly; Hughes, Richard K.; Sklenář, Jan; Win, Joe; Menke, Frank L.H.; Findlay, Kim; Banfield, Mark J.; Kamoun, Sophien; Bozkurt, Tolga O.

doi:10.7554/elife.10856

Cited by 200 publications

(296 citation statements)

References 49 publications

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“…). Notably, manipulation of selective autophagy by the host‐targeted P. infestans effector PexRD54 is also based on a disordered C‐terminal peptide that is stabilized by five tandem WY domains (Dagdas et al ., ; Maqbool et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL‐INDUCED CELL DEATH1

et al. 2018

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Summary The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL‐INDUCED CELL DEATH1 (RCD1).We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes.We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)‐induced defense genes and alters plant growth responses to light. HaRxL106‐mediated suppression of immunity is abolished in RCD1 loss‐of‐function mutants. We report that RCD1‐type proteins are phosphorylated, and we identified Mut9‐like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1‐interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA‐induced defense marker gene expression compared with wild‐type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling.Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.

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Section: Discussionmentioning

confidence: 99%

Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL‐INDUCED CELL DEATH1

et al. 2018

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“…Given that PexRD54 promotes autophagy, the story of its role in infection may extend beyond the observed exclusion of joka2 from autophagosomes [52 •• ]. Recently, P. infestans RXLR effectors have also been shown to target host proteins whose activity can play a positive role in promoting disease; so-called susceptibility (S) factors [53].…”

Section: Sites Of Action Targets and Recognition Of Rxlr Effectors Imentioning

confidence: 99%

The cell biology of late blight disease

Whisson

Boevink

Wang

et al. 2016

Current Opinion in Microbiology

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“…In plants, autophagy was shown to control hormone levels and signaling in basal resistance to hemibiotrophic bacteria and necrotrophic fungi and to regulate defense-and disease-associated cell death (16). In addition, the recent identification of an ATG8-binding oomycete effector that antagonizes the autophagy cargo receptor NEIGHBOR OF BRCA1 (NBR1)/JOKA2 suggests an important role of selective autophagy in plant immune responses (17). However, the molecular mechanisms and functions of autophagy in the regulation of immunity and pathogenesis during compatible plant virus infections remain largely unknown.…”

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confidence: 99%

Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

Hafrén

Macia

Love

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

231

308

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Autophagy plays a paramount role in mammalian antiviral immunity including direct targeting of viruses and their individual components, and many viruses have evolved measures to antagonize or even exploit autophagy mechanisms for the benefit of infection. In plants, however, the functions of autophagy in host immunity and viral pathogenesis are poorly understood. In this study, we have identified both anti-and proviral roles of autophagy in the compatible interaction of cauliflower mosaic virus (CaMV), a double-stranded DNA pararetrovirus, with the model plant Arabidopsis thaliana. We show that the autophagy cargo receptor NEIGHBOR OF BRCA1 (NBR1) targets nonassembled and virus particle-forming capsid proteins to mediate their autophagy-dependent degradation, thereby restricting the establishment of CaMV infection. Intriguingly, the CaMV-induced virus factory inclusions seem to protect against autophagic destruction by sequestering capsid proteins and coordinating particle assembly and storage. In addition, we found that virus-triggered autophagy prevents extensive senescence and tissue death of infected plants in a largely NBR1-independent manner. This survival function significantly extends the timespan of virus production, thereby increasing the chances for virus particle acquisition by aphid vectors and CaMV transmission. Together, our results provide evidence for the integration of selective autophagy into plant immunity against viruses and reveal potential viral strategies to evade and adapt autophagic processes for successful pathogenesis. A utophagy is a conserved intracellular pathway that engages specialized double-membrane vesicles, called "autophagosomes," to enclose and transport cytoplasmic content to lytic compartments for degradation and subsequent recycling (1). Autophagosome formation relies on extensive membrane rearrangements and is mediated by the concerted action of a core set of autophagy-related proteins (ATGs) (2, 3). At basal levels, autophagy serves mainly housekeeping functions in cellular homeostasis, whereas stimulated autophagy activity facilitates adaptation to developmental and environmental stress conditions including starvation, aging, and pathogen infection (1, 4). Ample evidence now indicates that autophagy, initially recognized as a mainly bulk catabolic process, is able specifically to target and degrade a multitude of cellular structures ranging from individual and aggregated proteins to entire organelles and invading microbes (5, 6). Selectivity is provided by a growing number of autophagic adaptor or receptor proteins identified in eukaryotic organisms that recruit the cargo to the developing autophagosome through interaction with membrane-associated ATG8/LC3 proteins (7, 8). Several mammalian autophagy receptors have been implicated in the targeting of intracellular bacterial and viral pathogens in a process called "xenophagy" (8-10). For instance, the cargo receptor p62 (SQSTM1) was shown to bind directly to and mediate autophagic clearance of different viral capsid pr...

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An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor

Cited by 200 publications

References 49 publications

Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL‐INDUCED CELL DEATH1

Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL‐INDUCED CELL DEATH1

The cell biology of late blight disease

Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

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