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Article ; Online: Isolation and Characterization of Plant Metabolite Signals that Induce Type III Secretion by the Plant Pathogen Pseudomonas syringae.

Rogan, Conner J / Anderson, Jeffrey C

Methods in molecular biology (Clifton, N.J.)

2019 Volume 1991, Page(s) 115–126

Abstract: Pseudomonas syringae is a bacterium that can cause disease on a wide range of plant species including important agricultural crops. A primary virulence mechanism used by P. syringae to infect host plants is the type III secretion system (T3SS), a syringe- ...

Abstract	Pseudomonas syringae is a bacterium that can cause disease on a wide range of plant species including important agricultural crops. A primary virulence mechanism used by P. syringae to infect host plants is the type III secretion system (T3SS), a syringe-like structure that delivers defense-suppressing proteins directly into plant cells. Genes encoding the T3SS are not transcribed in P. syringae prior to contact with a potential host plant and must be expressed during initial stages of infection. Specific organic and amino acids exuded by plants were recently identified as signals that can induce expression of T3SS-associated genes. Here we describe a technique to produce exudates from intact Arabidopsis seedlings and evaluate the exudates for the presence of these bioactive metabolites. We provide procedures for exudate production as well as downstream assays to assess T3SS gene expression using a GFP transcriptional reporter. We also describe methods for preparing high-quality protein and RNA from exudate-treated bacteria to directly assess changes in mRNA and protein abundance. These methods could be used to investigate mechanisms regulating P. syringae perception of plant metabolites as well as the release of these substances by the plant, and more generally to investigate host signals perceived by other phytopathogens.
MeSH term(s)	Amino Acids/pharmacology ; Arabidopsis/growth & development ; Arabidopsis/metabolism ; Arabidopsis/microbiology ; Bacterial Proteins/drug effects ; Bacterial Proteins/metabolism ; Gene Expression Regulation, Bacterial/drug effects ; Plant Diseases/microbiology ; Pseudomonas syringae/physiology ; Type III Secretion Systems/drug effects ; Type III Secretion Systems/metabolism
Chemical Substances	Amino Acids ; Bacterial Proteins ; Type III Secretion Systems
Language	English
Publishing date	2019-04-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-9458-8_13
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Article: Potato Non-Specific Lipid Transfer Protein StnsLTPI.33 Is Associated with the Production of Reactive Oxygen Species, Plant Growth, and Susceptibility to

Bvindi, Carol / Howe, Kate / Wang, You / Mullen, Robert T / Rogan, Conner J / Anderson, Jeffrey C / Goyer, Aymeric

Plants (Basel, Switzerland)

2023 Volume 12, Issue 17

Abstract: Plant non-specific lipid transfer proteins (nsLTPs) are small proteins capable of transferring phospholipids between membranes and binding non-specifically fatty acids in vitro. They constitute large gene families in plants, e.g., 83 in potato ( ...

Abstract	Plant non-specific lipid transfer proteins (nsLTPs) are small proteins capable of transferring phospholipids between membranes and binding non-specifically fatty acids in vitro. They constitute large gene families in plants, e.g., 83 in potato (
Language	English
Publishing date	2023-08-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2704341-1
ISSN	2223-7747
ISSN	2223-7747
DOI	10.3390/plants12173129
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Article: Development of a

Yan, Qing / Rogan, Conner J / Anderson, Jeffrey C

Molecular plant-microbe interactions : MPMI

2019 Volume 32, Issue 5, Page(s) 527–539

Abstract: The importance of pattern-triggered immunity (PTI) in plant defense has been clearly established through genetic studies of mutants lacking functional pattern recognition receptors (PRRs) and signaling components downstream of PRR activation. Despite ... ...

Abstract	The importance of pattern-triggered immunity (PTI) in plant defense has been clearly established through genetic studies of mutants lacking functional pattern recognition receptors (PRRs) and signaling components downstream of PRR activation. Despite extensive knowledge of PRR-mediated signaling responses to pathogen-associated molecular patterns (PAMPs), little is known about which of these responses, if any, are directly responsible for limiting bacterial growth. In this work, we established a protocol for coculturing the bacterial pathogen
MeSH term(s)	Arabidopsis/microbiology ; Arabidopsis Proteins ; Bacterial Proteins/genetics ; Bacteriological Techniques/methods ; Gene Expression Regulation, Bacterial ; Host-Pathogen Interactions/immunology ; Plant Diseases/microbiology ; Pseudomonas syringae/physiology ; Receptors, Pattern Recognition/genetics ; Type III Secretion Systems/immunology
Chemical Substances	Arabidopsis Proteins ; Bacterial Proteins ; Receptors, Pattern Recognition ; Type III Secretion Systems
Language	English
Publishing date	2019-03-29
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-10-18-0295-FI
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Article: Development of a Pseudomonas syringae–Arabidopsis Suspension Cell Infection System for Investigating Host Metabolite-Dependent Regulation of Type III Secretion and Pattern-Triggered Immunity

Yan, Qing / Rogan, Conner J / Anderson, Jeffrey C

Molecular plant-microbe interactions. 2019 May, v. 32, no. 5

2019

Abstract	The importance of pattern-triggered immunity (PTI) in plant defense has been clearly established through genetic studies of mutants lacking functional pattern recognition receptors (PRRs) and signaling components downstream of PRR activation. Despite extensive knowledge of PRR-mediated signaling responses to pathogen-associated molecular patterns (PAMPs), little is known about which of these responses, if any, are directly responsible for limiting bacterial growth. In this work, we established a protocol for coculturing the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 and Arabidopsis suspension cells. The system closely mirrors infection processes that occur in leaves, with bacteria relying on the type III secretion system (T3SS) for maximal growth and PAMP-induced plant defenses effectively limiting bacterial growth. To demonstrate the utility of this system, we investigated the molecular basis of PAMP-induced growth inhibition and discovered that T3SS-associated genes are inhibited when DC3000 is cocultured with PAMP-treated plant suspension cells. To determine the underlying mechanism of decreased T3SS gene expression, we performed metabolomics and biochemical analyses of suspension cell exudates and identified 14 metabolites that significantly increased or decreased following PAMP treatment. Citric acid, a known inducer of T3SS gene expression in DC3000, was among several organic acids decreased in exudates from PAMP-treated plant cells. Exogenous addition of citric acid increased T3SS gene expression and partially recovered growth of DC3000 in the presence of PAMP-treated cells, indicating that a portion of PAMP-induced defense in this system is decreased extracellular release of this metabolite. We envision that the well-defined infection conditions of this coculture system will be valuable for quantitative studies of type III effector delivery by P. syringae. Furthermore, this system provides a unique ‘top-down’ approach to unravel the molecular basis of PTI against P. syringae.
Keywords	Arabidopsis ; Pseudomonas syringae pv. tomato ; bacteria ; bacterial growth ; citric acid ; coculture ; gene expression ; genes ; growth retardation ; immunity ; leaves ; metabolites ; metabolomics ; mutants ; pathogen-associated molecular patterns ; pathogens ; receptors ; type III secretion system
Language	English
Dates of publication	2019-05
Size	p. 527-539.
Publishing place	Molecular Plant-Microbe Interactions
Document type	Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-10-18-0295-FI
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Article ; Online: Ancient co-option of an amino acid ABC transporter locus in Pseudomonas syringae for host signal-dependent virulence gene regulation.

Yan, Qing / Rogan, Conner J / Pang, Yin-Yuin / Davis, Edward W / Anderson, Jeffrey C

PLoS pathogens

2020 Volume 16, Issue 7, Page(s) e1008680

Abstract: Pathogenic bacteria frequently acquire virulence traits via horizontal gene transfer, yet additional evolutionary innovations may be necessary to integrate newly acquired genes into existing regulatory pathways. The plant bacterial pathogen Pseudomonas ... ...

Abstract	Pathogenic bacteria frequently acquire virulence traits via horizontal gene transfer, yet additional evolutionary innovations may be necessary to integrate newly acquired genes into existing regulatory pathways. The plant bacterial pathogen Pseudomonas syringae relies on a horizontally acquired type III secretion system (T3SS) to cause disease. T3SS-encoding genes are induced by plant-derived metabolites, yet how this regulation occurs, and how it evolved, is poorly understood. Here we report that the two-component system AauS-AauR and substrate-binding protein AatJ, proteins encoded by an acidic amino acid-transport (aat) and -utilization (aau) locus in P. syringae, directly regulate T3SS-encoding genes in response to host aspartate and glutamate signals. Mutants of P. syringae strain DC3000 lacking aauS, aauR or aatJ expressed lower levels of T3SS genes in response to aspartate and glutamate, and had decreased T3SS deployment and virulence during infection of Arabidopsis. We identified an AauR-binding motif (Rbm) upstream of genes encoding T3SS regulators HrpR and HrpS, and demonstrated that this Rbm is required for maximal T3SS deployment and virulence of DC3000. The Rbm upstream of hrpRS is conserved in all P. syringae strains with a canonical T3SS, suggesting AauR regulation of hrpRS is ancient. Consistent with a model of conserved function, an aauR deletion mutant of P. syringae strain B728a, a bean pathogen, had decreased T3SS expression and growth in host plants. Together, our data suggest that, upon acquisition of T3SS-encoding genes, a strain ancestral to P. syringae co-opted an existing AatJ-AauS-AauR pathway to regulate T3SS deployment in response to specific host metabolite signals.
MeSH term(s)	Arabidopsis/microbiology ; Gene Expression Regulation, Bacterial/physiology ; Plant Diseases/microbiology ; Pseudomonas syringae/pathogenicity ; Type III Secretion Systems/physiology ; Virulence/physiology
Chemical Substances	Type III Secretion Systems
Language	English
Publishing date	2020-07-16
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1008680
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Article ; Online: Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity.

Garner, Christopher M / Spears, Benjamin J / Su, Jianbin / Cseke, Leland J / Smith, Samantha N / Rogan, Conner J / Gassmann, Walter

PLoS genetics

2021 Volume 17, Issue 2, Page(s) e1009026

Abstract: Regulation of the plant immune system is important for controlling the specificity and amplitude of responses to pathogens and in preventing growth-inhibiting autoimmunity that leads to reductions in plant fitness. In previous work, we reported that ... ...

Abstract	Regulation of the plant immune system is important for controlling the specificity and amplitude of responses to pathogens and in preventing growth-inhibiting autoimmunity that leads to reductions in plant fitness. In previous work, we reported that SRFR1, a negative regulator of effector-triggered immunity, interacts with SNC1 and EDS1. When SRFR1 is non-functional in the Arabidopsis accession Col-0, SNC1 levels increase, causing a cascade of events that lead to autoimmunity phenotypes. Previous work showed that some members of the transcriptional co-repressor family TOPLESS interact with SNC1 to repress negative regulators of immunity. Therefore, to explore potential connections between SRFR1 and TOPLESS family members, we took a genetic approach that examined the effect of each TOPLESS member in the srfr1 mutant background. The data indicated that an additive genetic interaction exists between SRFR1 and two members of the TOPLESS family, TPR2 and TPR3, as demonstrated by increased stunting and elevated PR2 expression in srfr1 tpr2 and srfr1 tpr2 tpr3 mutants. Furthermore, the tpr2 mutation intensifies autoimmunity in the auto-active snc1-1 mutant, indicating a novel role of these TOPLESS family members in negatively regulating SNC1-dependent phenotypes. This negative regulation can also be reversed by overexpressing TPR2 in the srfr1 tpr2 background. Similar to TPR1 that positively regulates snc1-1 phenotypes by interacting with SNC1, we show here that TPR2 directly binds the N-terminal domain of SNC1. In addition, TPR2 interacts with TPR1 in vivo, suggesting that the opposite functions of TPR2 and TPR1 are based on titration of SNC1-TPR1 complexes by TPR2 or altered functions of a SNC1-TPR1-TPR2 complex. Thus, this work uncovers diverse functions of individual members of the TOPLESS family in Arabidopsis and provides evidence for the additive effect of transcriptional and post-transcriptional regulation of SNC1.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/immunology ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Autoimmunity/genetics ; Gene Expression Regulation, Plant/genetics ; Gene Expression Regulation, Plant/immunology ; Molecular Chaperones/genetics ; Molecular Chaperones/metabolism ; Mutation ; Plant Immunity/genetics ; Plants, Genetically Modified ; Up-Regulation
Chemical Substances	AT1G04130 protein, Arabidopsis ; Arabidopsis Proteins ; Molecular Chaperones ; SNC1 protein, Arabidopsis ; SRFR1 protein, Arabidopsis ; topless protein, Arabidopsis ; topless-related 1 protein, Arabidopsis
Language	English
Publishing date	2021-02-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1009026
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Article ; Online: Chronic blue light leads to accelerated aging in Drosophila by impairing energy metabolism and neurotransmitter levels.

Yang, Jun / Song, Yujuan / Law, Alexander D / Rogan, Conner J / Shimoda, Kelsey / Djukovic, Danijel / Anderson, Jeffrey C / Kretzschmar, Doris / Hendrix, David A / Giebultowicz, Jadwiga M

Frontiers in aging

2022 Volume 3, Page(s) 983373

Abstract: Blue light (BL) is becoming increasingly prevalent in artificial illumination, raising concerns about its potential health hazard to humans. In fact, there is evidence suggesting that acute BL exposure may lead to oxidative stress and death of retinal ... ...

Abstract	Blue light (BL) is becoming increasingly prevalent in artificial illumination, raising concerns about its potential health hazard to humans. In fact, there is evidence suggesting that acute BL exposure may lead to oxidative stress and death of retinal cells specialized for photoreception. On the other hand, recent studies in
Language	English
Publishing date	2022-08-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	3076785-4
ISSN	2673-6217 ; 2673-6217
ISSN (online)	2673-6217
ISSN	2673-6217
DOI	10.3389/fragi.2022.983373
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Article ; Online: StPIP1, a PAMP-induced peptide in potato, elicits plant defenses and is associated with disease symptom severity in a compatible interaction with Potato virus Y.

Combest, Max M / Moroz, Natalia / Tanaka, Kiwamu / Rogan, Conner J / Anderson, Jeffrey C / Thura, Lin / Rakotondrafara, Aurélie M / Goyer, Aymeric

Journal of experimental botany

2020 Volume 72, Issue 12, Page(s) 4472–4488

Abstract: The role of small secreted peptides in plant defense responses to viruses has seldom been investigated. Here, we report a role for potato (Solanum tuberosum) PIP1, a gene predicted to encode a member of the pathogen-associated molecular pattern (PAMP)- ... ...

Abstract	The role of small secreted peptides in plant defense responses to viruses has seldom been investigated. Here, we report a role for potato (Solanum tuberosum) PIP1, a gene predicted to encode a member of the pathogen-associated molecular pattern (PAMP)-induced peptide (PIP) family, in the response of potato to Potato virus Y (PVY) infection. We show that exogenous application of synthetic StPIP1 to potato leaves and nodes increased the production of reactive oxygen species and the expression of plant defense-related genes, revealing that StPIP1 triggers early defense responses. In support of this hypothesis, transgenic potato plants that constitutively overexpress StPIP1 had higher levels of leaf callose deposition and, based on measurements of viral RNA titers, were less susceptible to infection by a compatible PVY strain. Interestingly, systemic infection of StPIP1-overexpressing lines with PVY resulted in clear rugose mosaic symptoms that were absent or very mild in infected non-transgenic plants. A transcriptomics analysis revealed that marker genes associated with both pattern-triggered immunity and effector-triggered immunity were induced in infected StPIP1 overexpressors but not in non-transgenic plants. Together, our results reveal a role for StPIP1 in eliciting plant defense responses and in regulating plant antiviral immunity.
Language	English
Publishing date	2020-12-06
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erab078
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Article ; Online: Pathogen-induced AdDjSKI of the wild peanut, Arachis diogoi, potentiates tolerance of multiple stresses in E. coli and tobacco.

Rampuria, Sakshi / Bag, Pushan / Rogan, Conner J / Sharma, Akanksha / Gassmann, Walter / Kirti, P B

Plant science : an international journal of experimental plant biology

2018 Volume 272, Page(s) 62–74

Abstract: A gene encoding a serine-rich DnaJIII protein called AdDjSKI that has a 4Fe-4S cluster domain was found to be differentially upregulated in the wild peanut, Arachis diogoi in its resistance responses against the late leaf spot causing fungal pathogen ... ...

Abstract	A gene encoding a serine-rich DnaJIII protein called AdDjSKI that has a 4Fe-4S cluster domain was found to be differentially upregulated in the wild peanut, Arachis diogoi in its resistance responses against the late leaf spot causing fungal pathogen Phaeoisariopsis personata when compared with the cultivated peanut, Arachis hypogaea. AdDjSKI is induced in multiple stress conditions in A. diogoi. Recombinant E. coli cells expressing AdDjSKI showed better growth kinetics when compared with vector control cells under salinity, osmotic, acidic and alkaline stress conditions. Overexpression of this type three J-protein potentiates not only abiotic stress tolerance in Nicotiana tabacum var. Samsun, but also enhances its disease resistance against the phytopathogenic fungi Phytophthora parasitica pv nicotianae and Sclerotinia sclerotiorum. In the present study we show transcriptional upregulation of APX, Mn-SOD and HSP70 under heat stress and increased transcripts of PR genes in response to fungal infection. This transmembrane-domain-containing J protein displays punctate localization in chloroplasts. AdDjSKI appears to ensure proper folding of proteins associated with the photosynthetic machinery under stress.
MeSH term(s)	Arachis/genetics ; Arachis/physiology ; Disease Resistance/genetics ; Disease Resistance/physiology ; Escherichia coli/genetics ; Escherichia coli/physiology ; Organisms, Genetically Modified ; Osmotic Pressure/physiology ; Plant Proteins/genetics ; Plant Proteins/physiology ; Plants, Genetically Modified ; RNA, Plant/genetics ; Real-Time Polymerase Chain Reaction ; Salt Tolerance/genetics ; Salt Tolerance/physiology ; Stress, Physiological/genetics ; Stress, Physiological/physiology ; Nicotiana/genetics ; Nicotiana/physiology
Chemical Substances	Plant Proteins ; RNA, Plant
Language	English
Publishing date	2018-04-03
Publishing country	Ireland
Document type	Journal Article
ZDB-ID	742010-9
ISSN	1873-2259 ; 0168-9452
ISSN (online)	1873-2259
ISSN	0168-9452
DOI	10.1016/j.plantsci.2018.03.033
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Article ; Online: Arabidopsis

Kamiyama, Yoshiaki / Hirotani, Misaki / Ishikawa, Shinnosuke / Minegishi, Fuko / Katagiri, Sotaro / Rogan, Conner J / Takahashi, Fuminori / Nomoto, Mika / Ishikawa, Kazuya / Kodama, Yutaka / Tada, Yasuomi / Takezawa, Daisuke / Anderson, Jeffrey C / Peck, Scott C / Shinozaki, Kazuo / Umezawa, Taishi

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

2021 Volume 118, Issue 30

Abstract: The phytohormone abscisic acid (ABA) plays a major role in abiotic stress responses in plants, and subclass III SNF1-related protein kinase 2 (SnRK2) kinases mediate ABA signaling. In this study, we identified Raf36, a group C Raf-like protein kinase ... ...

Abstract	The phytohormone abscisic acid (ABA) plays a major role in abiotic stress responses in plants, and subclass III SNF1-related protein kinase 2 (SnRK2) kinases mediate ABA signaling. In this study, we identified Raf36, a group C Raf-like protein kinase in
MeSH term(s)	Abscisic Acid/pharmacology ; Arabidopsis/genetics ; Arabidopsis/growth & development ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Gene Expression Regulation, Plant/drug effects ; Phosphorylation ; Plant Growth Regulators/pharmacology ; Protein Serine-Threonine Kinases/genetics ; Protein Serine-Threonine Kinases/metabolism ; Signal Transduction ; Stress, Physiological
Chemical Substances	Arabidopsis Proteins ; Plant Growth Regulators ; SnRK2 protein, Arabidopsis ; Abscisic Acid (72S9A8J5GW) ; Protein Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2021-06-18
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.2100073118
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