Plant-Pathogen Interactions & Membrane Trafficking

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Cell-surface PTI and ETI, RLP-SOBIR1-BAK1 and downstream events

INF1 cell death but not Cf-4 cell death is reduced by Phytophthora infestans RxLR effector Pi02860 by targeting NPH3/RPT2-like 1 (NRL1), a ubiquitin E3 ligase independent of Avr3a Potato NPH3/RPT2-like protein StNRL1, targeted by a Phytophthora infestans RXLR effector, is a susceptibility factor - Yang et al. 2016 Plant Physiology

INF1 perception (RLP/SOBIR1 dependent, red.) leads to MAPK/WKRY-dependent gene induction of NbRBOHB, but flagellin perception (FLS2 dependent, red.) does not. The same regulatory elements (W-box) respond to R3a/Avr3a R-gene mediated immunity. Cell-surface- and cytosolic triggers going through the same! WRKY Transcription Factors Phosphorylated by MAPK Regulate a Plant Immune NADPH Oxidase in Nicotiana benthamiana - Adachi et al. 2015 The Plant Cell

Phytophthora infestans RXLR-WY Effector AVR3a Associates with Dynamin-Related Protein 2 Required for Endocytosis of the Plant Pattern Recognition Receptor FLS2 - Chaparro-Garcia et al. 2015 PLoS ONE

CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a - Gilroy et al. 2011 New Phytologist

PUB17 mediates FLS2 transcriptional and Cf-4 cell death responses, but not ELR responses, functioning in the nucleus U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans - He 2015 Journal of Experimental Botany

Review describing a bunch of RLPs in immunity that were shown to be genetically dependent on BAK1/SERK3, when no biochemical interaction was known yet. Two for all: receptor-associated kinases SOBIR1 and BAK1 - Liebrand et al. 2014 Trends in Plant Science

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Trafficking during plant-microbe interactions: Reviews

Protein trafficking during plant innate immunity - Wang et al. 2015 Journal of Integrative Plant Biology

Membrane trafficking pathways and their roles in plant–microbe interactions - Inada et al. 2014 Plant and Cell Physiology

A cellular backline: specialization of host membranes for defence - Faulkner 2015 Journal of Experimental Botany

A moving view: subcellular trafficking processes in pattern recognition receptor–triggered plant immunity - Ben Khaled et al. 2015 Annual Review of Phytopathology

Plasma membrane protein trafficking in plant–microbe interactions: a plant cell point of view - Leborgne-Castel and Bouhidel 2014 Frontiers in Plant Science 

Cell-autonomous defense, re-organization and trafficking of membranes in plant–microbe interactions - Dörmann et al. 2014 New Phytologist

Introduction to a Virtual Special Issue on cell biology at the plant–microbe interface - Panstruga and Kuhn 2015 New Phytologist

A highway for war and peace: the secretory pathway in plant–microbe interactions - Wang and Dong 2011 Molecular Plant

Plant exocytic secretion of toxic compounds for defense - Kwon and Yun 2014 Toxicological Research

Ready to fire: Secretion in plant immunity - Yun et al. 2008 Plant Signaling and Behavior

Dynamic cellular responses in plant–microbe interactions - Lipka and Panstruga 2005 Current Opinion in Plant Biology

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Karnik et al. 2015 The Plant Cell

The authors knew that regulatory element SEC11 binds secretory SNARE-protein SYP121/PEN1, but it was unknown through what kind of mechanism it actually regulates trafficking mediated by SYP121. Also, SYP122 is highly similar in structure and function compared to SYP121, but SEC11 turns out to very specifically work with SNARE-complexes containing SYP121 and not SYP122.

SEC11 is a Sec1/Munc18 protein. This SM family stabilizes SNARE complexes during vesicle fusion and regulates SNARE availability, which is well studied in animals and yeast.

Introducing the SYP121-N-terminus blocks secretory traffic, as can be marked by secreted YFP (secYFP)-retention in Arabidopsis root cells.

The authors demonstrate that SEC11 actively interacts with SYP121 and, by overexpression, can rescue blocked secretory traffic which is caused by the presence of the defective SYP121-N-terminus

More specificlly, SEC11 interacts with the N-terminus of endogenous SYP121, and this interaction is required for its ability to act on SYP121 to rescue secretory traffic defects, in this case when the defective SYP121-N-terminus is introduced.

In fact, a N-terminal mutation (L128R) in SEC11 disrupts secYFP secretory trafficking that is mediated by SYP121.

A truncated N-terminal version of SEC11 retains interaction with SYP121, but impairs SYP121 mediated secretory trafficking. secYFP was retained in wildtype plants expressing the SEC11-N-terminus, and unlike SEC11-full-length, SEC11-N-terminus could not rescue the traffic block caused by the defective SYP121-N-terminus.

Inducible SEC11-N-terminus expression furthermore lead to defects in cell expansion, placing these findings in a biological context.

Earlier evidence exists that SEC11 functions in ‘prepping’ SYP121 for membrane fusion, and also in assisting/stabilizing the subsequent SYP121-SNAP33-VAMP721 complex during actual membrane fusion: Arabidopsis Sec1/Munc18 protein SEC11 is a competitive and dynamic modulator of snare binding and SYP121-dependent vesicle traffic - Karnik et al. 2013 The Plant Cell

In tomato, SYP121 and SYP122 functionality was pried apart by studying the role of molecular switch Rab11a; the authors of this study found that this Rab-GTPase functions with SYP122 but not SYP121. Does the same occur in Arabidopsis? Tomato Rab11a characterization evidenced a difference between SYP121-dependent and SYP122-dependent exocytosis - Rehman et al. 2008 Plant Cell Physiology

Secretory SNAREs function in plant defence:

PEN1/SYP121, SYP122, SNAP33 and vesicle-associated VAMP721 and VAMP722 participate in focal defensive secretion: Co-option of a default secretory pathway for plant immune responses - Kwon et al. 2008 Nature

VAMP721/722 vesicles even carry defensive compounds to the apoplast: The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes - Kim et al. 2014 The Plant Journal

A recent review on SNARE-mediated secretion in plant defence: Plant exocytic secretion of toxic compounds for defense - Kwon et al. 2014 Toxicology Research

A review of focal accumulation of SNARE proteins during defence responses in a process dubbed Transcytosis: internalization and targeted secretion of plasma-membrane localized proteins: Transcytosis shuts the door for an unwanted guest - Nielsen and Thordal-Christensen 2013 Trends in Plant Science

Outside of Arabidopsis, also wheat SNAREs are employed during trafficking processes in defence against stripe rust: Wheat TaNPSN SNARE homologues are involved in vesicle-mediated resistance to stripe rust (Puccinia striiformis f. sp. tritici) - Wang et al. 2014 Journal of Experimental Botany

SYP121/122, VAMP721/722 have roles besides mediating membrane fusion:

These SNAREs can have a role independent of their trafficking function: membrane-localized SYP121, but not SYP122, functions in ion flux across the plasma membrane: A Tripartite SNARE-K+ Channel Complex Mediates in Channel-Dependent K+ Nutrition in Arabidopsis - Honsbein et al. 2009 The Plant Cell

A novel motif essential for SNARE interaction with the K+ channel KC1 and channel gating in Arabidopsis - Grefen et al. 2010 The Plant Cell

Very much related, the vesicle-localized VAMP721 and VAMP722 also bind and modulate the activity of K+-channels, postulating a mechanism to link trafficking and membrane dynamics to ion flux and changes in osmotic value:The Arabidopsis R-SNARE VAMP721 interacts with KAT1 and KC1 K+ channels to moderate K+ current at the plasma membrane - Zhang et al. 2015 The Plant Cell

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Ilyas et al. 2015 Current Biology

Of the two tomato secreted proteases Pip1 and Rcr3, the latter works with cell-surface receptor-like protein Cf-2.

A protease that did not co-evolve with Cf-2, Rcr3(lyc), causes necrosis in the presence of Cf-2, while a co-evolved Rcr3(pim) does not.

This corresponds nicely to findings in: Affinity of Avr2 for tomato cysteine protease Rcr3 correlates with the Avr2-triggered Cf-2-mediated hypersensitive response - Van ‘t Klooster et al. 2011 Molecular Plant Pathology

Pip1 contributes to tomato Cladosporium fulvum and PstDC3000 resistance, but is not the one 'guarded' by Cf-2

Rcr3 does not contribute to immunity vs C. fulvum or PstDC3000, but confers some immunity vs Phytophthora infestans. However, against P. infestans, the other protease Pip1 confers more resistance.

According to current definitions, Rcr3 is therefore both guardee and decoy, dependent on the pathogen (C. fulvum, decoy; P. infestans, guardee).

Rcr3 still has protease activity, which makes it less suited to fit the 'decoy' definition.

The authors speculate on the evolutionary history: Cf-2 is probably younger than Rcr3 and could have evolved to guard it. Alternatively, Rcr3 and Pip1 diverged, and Rcr3 could be currently under selectiong to become the 'decoy' for C. fulvum/PstDC3000 effectors.

More about Cf-2/Rcr3/Avr2:

Rcr3 from a wild tomato relative is under balancing selection, undergoing gene duplications and showing variation. Probably because of pathogen selection pressures, variants of Rcr3 are actively maintained in the tomato population, but because it is a ‘guarded’ protein, variation has consequences for its spontaneous activation of the guard: Cf-2. Balancing selection at the tomato RCR3 Guardee gene family maintains variation in strength of pathogen defense - Hörger et al. 2012 PLoS Genetics 

Rcr3(pim) is not only the target of C. fulvum Avr2, but also the nematode Globodera rostochiensis effector Gr-VAP1 which like Avr2 also triggers Cf-2, and filamentous oomycete pathogen Phytophthora infestans effectors EPIC1 and EPIC2b of which the effects do not trigger Cf-2:

Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode - Lozano-Torres et al. 2012 Proceedings of the National Academy of Sciences

Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3 - Song et al. 2009 Proceedings of the National Academy of Sciences

Novel mutations detected in avirulence genes overcoming tomato Cf resistance genes in isolates of a Japanese population of Cladosporium fulvum - Iida et al. 2015 PLoS ONE

Recognitional specificity and evolution in the tomato–Cladosporium fulvum pathosystem - Wulff et al. 2009 Molecular Plant-Microbe Interactions

The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense - Van Esse et al. 2008 The Plant Cell

Cladosporium fulvum Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance - Rooney et al. 2005 Science

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SOBIR1 literature

Research papers:

https://www.ncbi.nlm.nih.gov/pubmed/27995670

Tomato CuRe (RLP) interacts with SOBIR1 and detects parasitic plant factors (Cuscuta factors). Detection of the plant parasite Cuscuta reflexa by a tomato cell surface receptor - Hegenauer et al. 2016 Science

Loss-of-function of Arabidopsis receptor-like kinase BIR1 activates cell death and defense responses mediated by BAK1 and SOBIR1 - Liu et al. 2016 New Phytologist

SOBIR1 contributes to non-host resistance to Magnaporthe oryzae in Arabidopsis - Takahashi et al. 2016 Biosci Biotechnol Biochem

OMVs induce defense responses in a SOBIR1- and BAK1-dependent manner: Bacterial Outer Membrane Vesicles Induce Plant Immune Responses - Bahar et al. 2016 Molecular Plant-Microbe Interactions

NbCSPR (N. benthamiana bacterial cold shock protein receptor-like protein), was found to bind and detect bacterial csp22, it associates with NbSOBIR1 but, strikingly, does not depend on it for signaling (VIGS; other RLPs like Cf-4 and Ve1 do). Accumulation is affected by NbSOBIR1 silencing. NbSOBIR1 and NbBAK1 weakly associated before csp22, but strongly after csp22. NbCSPR responses lead to BAK1 recruitment and are BAK1 dependent.  NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana - Saur et al. 2016 Proceedings of the National Academy of Sciences

RLP23 interacts with SOBIR1, recruits BAK1 upon NLP (nlp20) perception. An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity - Albert et al. 2015 Nature Plants

ELR detects INF1 and interacts with BAK1 and SOBIR1. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato - Du et al. 2015 Nature Plants, and Potato SOBIR1 and SOBIR1-like interact with the elicitin-response receptor (ELR) of potato and are involved in the response to INF1 elicitin of Phytophthora infestans - Domazakis et al. 2014 XVI-MPMI Conference Abstracts

Brassica napus LepR3 (RLP) interacts with BnSOBIR1. NbSOBIR1 and NbSERK3 required for AvrLm1-triggered LepR3 output. The receptor-like kinase SOBIR1 interacts with Brassica napus LepR3 and is required for Leptosphaeria maculans AvrLm1-triggered immunity - Ma and Hossein Borhan 2015 Frontiers in Plant Science

An overdose of the Arabidopsis coreceptor BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE1 or its ectodomain causes autoimmunity in a SUPPRESSOR OF BIR1-1-dependent manner - Domínguez-Ferreras et al. 2015 Plant Physiology

SOBIR1 requires the GxxxG dimerization motif in its transmembrane domain to form constitutive complexes with receptor-like proteins - Bi et al. 2015 Molecular Plant Pathology

UGGT (ERQC) is required for biogenesis of AtSOBIR1:  ER Quality Control Components UGGT and STT3a are required for activation of defense responses in bir1-1 - Zhang et al. 2015 PLoS ONE

P. parasitica ParA1-triggered cell death requires SlSOBIR1:  Tomato SOBIR1/EVR homologs are involved in elicitin perception and plant defense against the oomycete pathogen Phytophthora parasitica - Peng et al. 2015 Molecular Plant Microbe Interactions

B. napus RLM2 (RLP) interacts with SOBIR1: The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus - Larkan et al. 2015 Plant Biotechnology Journal

Arabidopsis thaliana receptor-like protein AtRLP23 associates with the receptor-like kinase AtSOBIR1 - Bi et al. 2014 Plant Signaling and Behavior

Ve1 and Ve2 (RLPs) interact with SlSOBIR1: Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2 - Fradin et al. 2014 PLoS ONE

Regulation of SOBIR1 accumulation and activation of defense responses in bir1–1 by specific components of ER quality control - Sun et al. 2014 The Plant Journal

RBPG1 (RLP) interacts with PGs and AtSOBIR1, is dependent on AtSOBIR1: Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1 - Zhang et al. 2014 Plant Physiology

ReMAX (RLP) signals in a AtSOBIR1-dependent manner: Perception of the novel MAMP eMax from different Xanthomonas species requires the Arabidopsis receptor-like protein ReMAX and the receptor kinase SOBIR - Jehle et al. 2013 Plant Signaling & Behavior

RLP30 detects SCFE1 from Sclerotinia sclerotum, interacts with and is dependent on AtSOBIR1: Arabidopsis RECEPTOR-LIKE PROTEIN30 and receptor-like kinase SUPPRESSOR OF BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi - Zhang et al. 2013 The Plant Cell

Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection - Liebrand et al. 2013 Proceedings of the National Academy of Sciences

Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis - Gao et al. 2009 Cell Host and Microbe

Induced expression of a temperature-sensitive leucine-rich receptor-like protein kinase gene by hypersensitive cell death by hypersensitive cell death and wounding in tobacco plant carrying the N resistance gene - Ito et al. 2002 Plant and Cell Physiology

Review papers:

Should I stay or should I go? Traffic control for plant pattern recognition receptors - Frescatada-Rosa et al. 2015 Current Opinion in Plant Biology

A moving view: subcellular trafficking processes in pattern recognition receptor–triggered plant immunity - Ben Khaled et al. 2015 Annual Review of Phytopathology

Receptor like proteins associate with SOBIR1-type of adaptors to form bimolecular receptor kinases - Gust and Felix 2015 Current Opinion in Plant Biology

Two for all: receptor-associated kinases SOBIR1 and BAK1 - Liebrand et al. 2014 Trends in Plant Science

Effector-triggered defence against apoplastic fungal pathogens - Stotz et al 2014 Trends in Plant Science

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Chakrabarti et al. 2015 - Molecular Plant Pathology

The membrane-proximal region of the cytosolic domain of Cf-9 plays an important role in Cf-9-mediated necrosis

An alanine mutation of T835 had no effect on Cf-9 function but an aspartic acid mutation, which mimics phosphorylation, reduced Cf-9 function 

Phosphorylation/de-phosphorylation of T835 could act as a molecular switch to determine whether Cf-9 is in a primed or inactive state 

The cytosolic domain of Cf-9 interacts with the cytosolic domain of tomato VAP27 

This interaction could be disrupted by an alanine mutation of P838, whereas interaction with CITRX remained unaffected 

The authors tweaked the putative endocytic motif ‘YPAW’ (YxxPHI, interacts with AP-2 clathrin adapters in animal cells) to more resemble YxxPHI, and found no difference in receptor abundance, but a reduction in Avr9-induced necrosis. Does this rule out a role for the YxxPHI motif in receptor endocytosis? Localization data is not available.

More about Cf-9 players ACIK1, CITRX, VAP27 and ACRE276:

Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato - Rowland et al. 2005 The Plant Cell

CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence - Rivas et al. 2004 The EMBO Journal

CITRX thioredoxin is a putative adaptor protein connecting Cf-9 and the ACIK1 protein kinase during the Cf-9/Avr9- induced defence response - Nekrasov et al. 2006 FEBS Letters

Molecular cloning and partial characterization of a plant VAP33 homologue with a major sperm protein domain - Laurent et al. 2000 Biochem Biophys Res Commun

The E3 ubiquitin ligase activity of arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense - Yang et al. 2006 The Plant Cell

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Kalinowska et al. 2015 - Proceedings of the National Academy of Sciences

ALIX can directly interact with AMSH3

alix null mutants show similar phenotypes to amsh3

ALIX Is required for vacuole biogenesis

AMSH3 shows colocalization with late endosomal markers ARA6/7

AMSH3 and ALIX colocalize on late endosomes

ALIX binds ubiquitin and is involved in ubiquitin-dependent protein degradation

ALIX Is important for localization of AMSH3 on ARA7-labeled vesicles

This related study published a couple of days later describes that ALIX interacts with ESCRT-III component SNF7 on late endosomes/MVBs. The authors also independently found ALIX involvement in vacuole biogenesis, and interestingly also in vacuolar trafficking of the RLK BRI1, and plasma membrane-localized phosphate transporter PHT1: ESCRT-III-associated protein ALIX mediates high affinity phosphate transporter trafficking to maintain phosphate homeostasis in Arabidopsis - Cardona-López et al. 2015 The Plant Cell

More about AMSH3/ESCRT-III:

The Arabidopsis deubiquitinating enzyme AMSH3 interacts with ESCRT-III subunits and regulates their localization - Katsiarimpa et al. 2011 The Plant Cell

The ESCRT-III-interacting deubiquitinating enzyme AMSH3 is essential for degradation of ubiquitinated membrane proteins in Arabidopsis thaliana - Katsiarimpa et al. 2014 Plant & Cell Physiology

Proper AMSH3 interaction with ESCRT-III components and K63-linked deubiquitinase activity is required for defense - Schulz-Larsen et al. 2014 XVI IS-MPMI, Rhodes, Greece

Arabidopsis Endosomal Sorting Complex Required for Transport III (ESCRT-III) regulates internal vesicle formation of prevacuolar compartment and is required for plant development - Cai et al. 2014 Plant Physiology

More about MVB biogenesis and maturation:

Biogenesis of plant prevacuolar multivesicular bodies - Cui et al. 2016 Molecular Plant

Phosphatidylinositol 3-phosphate 5-kinase, FAB1/PIKfyve mediates endosome maturation to establish endosome-cortical microtubule interaction in Arabidopsis - Hirano et al. 2015 Plant Physiology

FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis - Kolb et al. 2015 Plant Physiology

A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth - Gao et al. 2014 Current Biology

A critical role of LIP5, a positive regulator of multivesicular body biogenesis, in plant responses to heat and salt stresses - Wang et al. 2015 Plant Physiology

Arabidopsis LIP5, a positive regulator of multivesicular body biogenesis, is a critical target of pathogen-responsive MAPK cascade in plant basal defense - Wang et al. 2014 PLoS Pathogens