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Article ; Online: A RabGAP negatively regulates plant autophagy and immune trafficking.

Yuen, Enoch Lok Him / Leary, Alexandre Y / Clavel, Marion / Tumtas, Yasin / Mohseni, Azadeh / Zhao, Jierui / Picchianti, Lorenzo / Jamshidiha, Mostafa / Pandey, Pooja / Duggan, Cian / Cota, Ernesto / Dagdas, Yasin / Bozkurt, Tolga O

Current biology : CB

2024

Abstract: Plants rely on autophagy and membrane trafficking to tolerate stress, combat infections, and maintain cellular homeostasis. However, the molecular interplay between autophagy and membrane trafficking is poorly understood. Using an AI-assisted approach, ... ...

Abstract	Plants rely on autophagy and membrane trafficking to tolerate stress, combat infections, and maintain cellular homeostasis. However, the molecular interplay between autophagy and membrane trafficking is poorly understood. Using an AI-assisted approach, we identified Rab3GAP-like (Rab3GAPL) as a key membrane trafficking node that controls plant autophagy negatively. Rab3GAPL suppresses autophagy by binding to ATG8, the core autophagy adaptor, and deactivating Rab8a, a small GTPase essential for autophagosome formation and defense-related secretion. Rab3GAPL reduces autophagic flux in three model plant species, suggesting that its negative regulatory role in autophagy is conserved in land plants. Beyond autophagy regulation, Rab3GAPL modulates focal immunity against the oomycete pathogen Phytophthora infestans by preventing defense-related secretion. Altogether, our results suggest that Rab3GAPL acts as a molecular rheostat to coordinate autophagic flux and defense-related secretion by restraining Rab8a-mediated trafficking. This unprecedented interplay between a RabGAP-Rab pair and ATG8 sheds new light on the intricate membrane transport mechanisms underlying plant autophagy and immunity.
Language	English
Publishing date	2024-04-22
Publishing country	England
Document type	Journal Article
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2024.04.002
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Article ; Online: Contrasting and emerging roles of autophagy in plant immunity.

Leary, Alexandre Y / Savage, Zachary / Tumtas, Yasin / Bozkurt, Tolga O

Current opinion in plant biology

2019 Volume 52, Page(s) 46–53

Abstract: Autophagy is a conserved eukaryotic process that mediates degradation and relocation of cellular material to maintain homeostasis and cope with cellular stress. Remarkably, this ancient catabolic machinery has been co-opted to eliminate invading ... ...

Abstract	Autophagy is a conserved eukaryotic process that mediates degradation and relocation of cellular material to maintain homeostasis and cope with cellular stress. Remarkably, this ancient catabolic machinery has been co-opted to eliminate invading pathogens in a variety of ways. Plant autophagy not only mediates selective destruction of viruses but also limits infection by extracellular bacterial and filamentous pathogens. The emerging paradigm is that autophagy adaptors, responsible for selective cargo sorting, have been appointed to counteract pathogen infection, while adapted pathogens have evolved to subvert the immune functions of the autophagic machinery. In this review, we discuss recent findings that contribute to understanding the role of autophagy in plant immunity and highlight key questions to address in the field moving forward.
MeSH term(s)	Autophagy ; Homeostasis ; Immunity, Innate ; Plant Immunity ; Plants ; Viruses
Language	English
Publishing date	2019-08-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1418472-2
ISSN	1879-0356 ; 1369-5266
ISSN (online)	1879-0356
ISSN	1369-5266
DOI	10.1016/j.pbi.2019.07.002
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Article: Contrasting and emerging roles of autophagy in plant immunity

Leary, Alexandre Y / Savage, Zachary / Tumtas, Yasin / Bozkurt, Tolga O

Current opinion in plant biology. 2019 Dec., v. 52

2019

Abstract	Autophagy is a conserved eukaryotic process that mediates degradation and relocation of cellular material to maintain homeostasis and cope with cellular stress. Remarkably, this ancient catabolic machinery has been co-opted to eliminate invading pathogens in a variety of ways. Plant autophagy not only mediates selective destruction of viruses but also limits infection by extracellular bacterial and filamentous pathogens. The emerging paradigm is that autophagy adaptors, responsible for selective cargo sorting, have been appointed to counteract pathogen infection, while adapted pathogens have evolved to subvert the immune functions of the autophagic machinery. In this review, we discuss recent findings that contribute to understanding the role of autophagy in plant immunity and highlight key questions to address in the field moving forward.
Keywords	autophagy ; homeostasis ; immune response ; pathogens
Language	English
Dates of publication	2019-12
Size	p. 46-53.
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	1418472-2
ISSN	1879-0356 ; 1369-5266
ISSN (online)	1879-0356
ISSN	1369-5266
DOI	10.1016/j.pbi.2019.07.002
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Article ; Online: Dynamic localization of a helper NLR at the plant-pathogen interface underpins pathogen recognition.

Duggan, Cian / Moratto, Eleonora / Savage, Zachary / Hamilton, Eranthika / Adachi, Hiroaki / Wu, Chih-Hang / Leary, Alexandre Y / Tumtas, Yasin / Rothery, Stephen M / Maqbool, Abbas / Nohut, Seda / Martin, Toby Ross / Kamoun, Sophien / Bozkurt, Tolga Osman

Proceedings of the National Academy of Sciences of the United States of America

2021 Volume 118, Issue 34

Abstract: Plants employ sensor-helper pairs of NLR immune receptors to recognize pathogen effectors and activate immune responses. Yet, the subcellular localization of NLRs pre- and postactivation during pathogen infection remains poorly understood. Here, we show ... ...

Abstract	Plants employ sensor-helper pairs of NLR immune receptors to recognize pathogen effectors and activate immune responses. Yet, the subcellular localization of NLRs pre- and postactivation during pathogen infection remains poorly understood. Here, we show that NRC4, from the "NRC" solanaceous helper NLR family, undergoes dynamic changes in subcellular localization by shuttling to and from the plant-pathogen haustorium interface established during infection by the Irish potato famine pathogen
MeSH term(s)	Cell Membrane/metabolism ; Disease Resistance/immunology ; Host-Pathogen Interactions ; NLR Proteins/genetics ; NLR Proteins/metabolism ; Phytophthora infestans/physiology ; Plant Diseases/immunology ; Plant Diseases/parasitology ; Plant Immunity/immunology ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Receptors, Immunologic/metabolism ; Nicotiana/immunology ; Nicotiana/metabolism ; Nicotiana/parasitology
Chemical Substances	NLR Proteins ; Plant Proteins ; Receptors, Immunologic
Language	English
Publishing date	2021-08-20
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2104997118
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Article ; Online: An oomycete effector subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface.

Pandey, Pooja / Leary, Alexandre Y / Tumtas, Yasin / Savage, Zachary / Dagvadorj, Bayantes / Duggan, Cian / Yuen, Enoch Lh / Sanguankiattichai, Nattapong / Tan, Emily / Khandare, Virendrasinh / Connerton, Amber J / Yunusov, Temur / Madalinski, Mathias / Mirkin, Federico Gabriel / Schornack, Sebastian / Dagdas, Yasin / Kamoun, Sophien / Bozkurt, Tolga O

eLife

2021 Volume 10

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 ...

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
MeSH term(s)	Autophagy ; Fungal Proteins/genetics ; Fungal Proteins/metabolism ; Host-Pathogen Interactions ; Phytophthora infestans/physiology ; Plant Diseases/microbiology ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Solanum tuberosum/genetics ; Solanum tuberosum/metabolism ; Solanum tuberosum/microbiology
Chemical Substances	Fungal Proteins ; Plant Proteins
Language	English
Publishing date	2021-08-23
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.65285
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Article ; Online: Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans.

Savage, Zachary / Duggan, Cian / Toufexi, Alexia / Pandey, Pooja / Liang, Yuxi / Segretin, María Eugenia / Yuen, Lok Him / Gaboriau, David C A / Leary, Alexandre Y / Tumtas, Yasin / Khandare, Virendrasinh / Ward, Andrew D / Botchway, Stanley W / Bateman, Benji C / Pan, Indranil / Schattat, Martin / Sparkes, Imogen / Bozkurt, Tolga O

The Plant journal : for cell and molecular biology

2021 Volume 107, Issue 6, Page(s) 1771–1787

Abstract: Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response ...

Abstract	Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1)-mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector-mediated suppression of BAK1-mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant-pathogen interactions.
MeSH term(s)	Actin Cytoskeleton/metabolism ; Actin Cytoskeleton/microbiology ; Bridged Bicyclo Compounds, Heterocyclic/pharmacology ; Chloroplasts/drug effects ; Chloroplasts/immunology ; Chloroplasts/microbiology ; Dinitrobenzenes/pharmacology ; Host-Pathogen Interactions/physiology ; Light ; Microscopy, Confocal ; Optical Tweezers ; Phytophthora infestans/pathogenicity ; Plant Diseases/microbiology ; Plant Immunity ; Plant Leaves/drug effects ; Plant Leaves/microbiology ; Plants, Genetically Modified ; Reactive Oxygen Species/metabolism ; Sulfanilamides/pharmacology ; Thiazolidines/pharmacology ; Nicotiana/drug effects ; Nicotiana/genetics ; Nicotiana/immunology ; Nicotiana/microbiology
Chemical Substances	Bridged Bicyclo Compounds, Heterocyclic ; Dinitrobenzenes ; Reactive Oxygen Species ; Sulfanilamides ; Thiazolidines ; oryzalin (662E385DWH) ; latrunculin A (SRQ9WWM084)
Language	English
Publishing date	2021-08-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.15416
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans

Savage, Zachary / Duggan, Cian / Toufexi, Alexia / Pandey, Pooja / Liang, Yuxi / Segretin, María Eugenia / Yuen, Lok Him / Gaboriau, David C. A. / Leary, Alexandre Y. / Tumtas, Yasin / Khandare, Virendrasinh / Ward, Andrew D. / Botchway, Stanley W. / Bateman, Benji C. / Pan, Indranil / Schattat, Martin / Sparkes, Imogen / Bozkurt, Tolga O.

plant journal. 2021 Sept., v. 107, no. 6

2021

Abstract	Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial compounds and associate with the nucleus through tubular extensions called stromules. Although it is well established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection‐triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1‐ASSOCIATED KINASE 1 (BAK1)‐mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense‐related induction of stromules, effector‐mediated suppression of BAK1‐mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant–pathogen interactions.
Keywords	Irish potato famine ; Phytophthora infestans ; actin ; brassinosteroids ; chloroplasts ; haustoria ; microfilaments ; pathogens ; photosynthesis ; polymerization
Language	English
Dates of publication	2021-09
Size	p. 1771-1787.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.15416
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen.

Dagdas, Yasin F / Pandey, Pooja / Tumtas, Yasin / Sanguankiattichai, Nattapong / Belhaj, Khaoula / Duggan, Cian / Leary, Alexandre Y / Segretin, Maria E / Contreras, Mauricio P / Savage, Zachary / Khandare, Virendrasinh S / Kamoun, Sophien / Bozkurt, Tolga O

eLife

2018 Volume 7

Abstract: During plant cell invasion, the ... ...

Abstract	During plant cell invasion, the oomycete
MeSH term(s)	ATPases Associated with Diverse Cellular Activities/genetics ; ATPases Associated with Diverse Cellular Activities/immunology ; Autophagosomes/immunology ; Autophagosomes/parasitology ; Autophagy/genetics ; Autophagy/immunology ; Autophagy-Related Protein 8 Family/genetics ; Autophagy-Related Protein 8 Family/immunology ; Carrier Proteins/genetics ; Carrier Proteins/immunology ; Gene Expression Regulation ; Host-Pathogen Interactions ; Membrane Proteins/genetics ; Membrane Proteins/immunology ; Phytophthora infestans/genetics ; Phytophthora infestans/growth & development ; Phytophthora infestans/pathogenicity ; Plant Cells/immunology ; Plant Cells/parasitology ; Plant Diseases/genetics ; Plant Diseases/immunology ; Plant Diseases/parasitology ; Plant Immunity/genetics ; Plant Proteins/genetics ; Plant Proteins/immunology ; Protein Binding ; Signal Transduction ; Solanum tuberosum/genetics ; Solanum tuberosum/immunology ; Solanum tuberosum/parasitology
Chemical Substances	Autophagy-Related Protein 8 Family ; Carrier Proteins ; Membrane Proteins ; Plant Proteins ; ATPases Associated with Diverse Cellular Activities (EC 3.6.4.-)
Language	English
Publishing date	2018-06-22
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.37476
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Article: Modulation of plant autophagy during pathogen attack

Leary, Alexandre Y / Sanguankiattichai, Nattapong / Duggan, Cian / Tumtas, Yasin / Pandey, Pooja / Segretin, Maria E / Salguero Linares, Jose / Savage, Zachary D / Yow, Rui Jin / Bozkurt, Tolga O / Bozhkov, Peter

Journal of experimental botany. 2018 Mar. 14, v. 69, no. 6

2018

Abstract: In plants, the highly conserved catabolic process of autophagy has long been known as a means of maintaining cellular homeostasis and coping with abiotic stress conditions. Accumulating evidence has linked autophagy to immunity against invading pathogens, ...

Abstract	In plants, the highly conserved catabolic process of autophagy has long been known as a means of maintaining cellular homeostasis and coping with abiotic stress conditions. Accumulating evidence has linked autophagy to immunity against invading pathogens, regulating plant cell death, and antimicrobial defences. In turn, it appears that phytopathogens have evolved ways not only to evade autophagic clearance but also to modulate and co-opt autophagy for their own benefit. In this review, we summarize and discuss the emerging discoveries concerning how pathogens modulate both host and self-autophagy machineries to colonize their host plants, delving into the arms race that determines the fate of interorganismal interaction.
Keywords	abiotic stress ; autophagy ; homeostasis ; host plants ; plant pathogens
Language	English
Dates of publication	2018-0314
Size	p. 1325-1333.
Publishing place	Oxford University Press
Document type	Article
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erx425
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Modulation of plant autophagy during pathogen attack.

Leary, Alexandre Y / Sanguankiattichai, Nattapong / Duggan, Cian / Tumtas, Yasin / Pandey, Pooja / Segretin, Maria E / Salguero Linares, Jose / Savage, Zachary D / Yow, Rui Jin / Bozkurt, Tolga O

Journal of experimental botany

2017 Volume 69, Issue 6, Page(s) 1325–1333

Abstract	In plants, the highly conserved catabolic process of autophagy has long been known as a means of maintaining cellular homeostasis and coping with abiotic stress conditions. Accumulating evidence has linked autophagy to immunity against invading pathogens, regulating plant cell death, and antimicrobial defences. In turn, it appears that phytopathogens have evolved ways not only to evade autophagic clearance but also to modulate and co-opt autophagy for their own benefit. In this review, we summarize and discuss the emerging discoveries concerning how pathogens modulate both host and self-autophagy machineries to colonize their host plants, delving into the arms race that determines the fate of interorganismal interaction.
MeSH term(s)	Autophagy/immunology ; Autophagy/physiology ; Host-Pathogen Interactions/immunology ; Plant Immunity ; Plants/immunology ; Plants/microbiology
Language	English
Publishing date	2017-11-29
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erx425
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