Global SUMOylome Adjustments in Basal Defenses of Arabidopsis thaliana Involve Complex Interplay Between SMALL-UBIQUITIN LIKE MODIFIERs and the Negative Immune Regulator SUPPRESSOR OF rps4-RLD1

Steady-state SUMOylome of a plant is adjusted locally during developmental transitions and more globally during stress exposures. We recently reported that basal immunity in Arabidopsis thaliana against Pseudomonas syringae pv tomato strain DC3000 (PstDC3000) is associated with strong enhancements in the net SUMOylome. Transcriptional upregulations of SUMO conjugases, suppression of protease, and increased SUMO translations accounted for this enhanced SUMOylation. Antagonistic roles of SUMO1/2 and SUMO3 isoforms further fine-tuned the SUMOylome adjustments, thus impacting defense amplitudes and immune outcomes. Loss of function of SUPPRESSOR OF rps4-RLD1 (SRFR1), a previously reported negative regulator of basal defenses, also caused constitutive increments in global SUMO-conjugates through similar modes. These suggest that SRFR1 plays a pivotal role in maintenance of SUMOylation homeostasis and its dynamic changes during immune elicitations. Here, we demonstrate that SRFR1 degradation kinetically precedes and likely provides the salicylic acid (SA) elevations necessary for the SUMOylome increments in basal defenses. We show that SRFR1 not only is a SUMOylation substrate but also interacts in planta with both SUMO1 and SUMO3. In sum1 or sum3 mutants, SRFR1 stabilities are reduced albeit by different modes. Whereas a srfr1 sum1 combination is lethal, the srfr1 sum3 plants retain developmental defects and enhanced immunity of the srfr1 parent. Together with increasing evidence of SUMOs self-regulating biochemical efficiencies of SUMOylation-machinery, we present their impositions on SRFR1 expression that in turn counter-modulates the SUMOylome. Overall, our investigations reveal multifaceted dynamics of regulated SUMOylome changes via SRFR1 in defense-developmental balance.

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Immunogold Labeling of Hrp Pili of Pseudomonas syringae pv. tomato Assembled in Minimal Medium and In Planta

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2001.14.2.234 ◽

2001 ◽

Vol 14 (2) ◽

pp. 234-241 ◽

Cited By ~ 25

Author(s):

Wenqi Hu ◽

Jing Yuan ◽

Qiao-Ling Jin ◽

Patrick Hart ◽

Sheng Yang He

Keyword(s):

Arabidopsis Thaliana ◽

Pseudomonas Syringae ◽

Minimal Medium ◽

Leaf Tissue ◽

Hypersensitive Reaction ◽

Immunogold Labeling ◽

Structural Protein ◽

In Planta ◽

Hrp Genes

Hypersensitive reaction and pathogenicity (hrp) genes are required for Pseudomonas syringae pv. tomato (Pst) DC3000 to cause disease in susceptible tomato and Arabidopsis thaliana plants and to elicit the hypersensitive response in resistant plants. The hrp genes encode a type III protein secretion system known as the Hrp system, which in Pst DC3000 secretes HrpA, HrpZ, HrpW, and AvrPto and assembles a surface appendage, named the Hrp pilus, in hrp-gene-inducing minimal medium. HrpA has been suggested to be the Hrp pilus structural protein on the basis of copurification and mutational analyses. In this study, we show that an antibody against HrpA efficiently labeled Hrp pili, whereas antibodies against HrpW and HrpZ did not. Immunogold labeling of bacteria-infected Arabidopsis thaliana leaf tissue with an Hrp pilus antibody revealed a characteristic lineup of gold particles around bacteria and/or at the bacterium-plant contact site. These results confirm that HrpA is the major structural protein of the Hrp pilus and provide evidence that Hrp pili are assembled in vitro and in planta.

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Identification of a putative DNA-binding protein in Arabidopsis that acts as a susceptibility hub and interacts with multiple Pseudomonas syringae effectors

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-10-20-0291-r ◽

2020 ◽

Author(s):

Karl Schreiber ◽

Jennifer D Lewis

Keyword(s):

Pseudomonas Syringae ◽

Transcriptional Profiling ◽

Effector Proteins ◽

Ribosomal Protein Genes ◽

Loss Of Function ◽

Wild Type ◽

In Planta ◽

Arabidopsis Protein ◽

Wide Range

Phytopathogens use secreted effector proteins to suppress host immunity and promote pathogen virulence, and there is increasing evidence that the host-pathogen interactome comprises a complex network. In an effort to identify novel interactors of the Pseudomonas syringae effector HopZ1a, we performed a yeast two-hybrid screen that identified a previously uncharacterized Arabidopsis protein that we designate HopZ1a Interactor 1 (ZIN1). Additional analyses in yeast and in planta revealed that ZIN1 also interacts with several other P. syringae effectors. We show that an Arabidopsis loss-of-function zin1 mutant is less susceptible to infection by certain strains of P. syringae, while overexpression of ZIN1 results in enhanced susceptibility. Functionally, ZIN1 exhibits topoisomerase-like activity in vitro. Transcriptional profiling of wild-type and zin1 Arabidopsis plants inoculated with P. syringae indicated that while ZIN1 regulates a wide range of pathogen-responsive biological processes, the list of genes more highly expressed in zin1 versus wild-type plants was particularly enriched for ribosomal protein genes. Altogether, these data illuminate ZIN1 as a potential susceptibility hub that interacts with multiple effectors to influence the outcome of plant-microbe interactions.

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Analysis of Resistance Gene-Mediated Defense Responses in Arabidopsis thaliana Plants Carrying a Mutation in CPR5

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.1998.11.12.1196 ◽

1998 ◽

Vol 11 (12) ◽

pp. 1196-1206 ◽

Cited By ~ 51

Author(s):

Jens Boch ◽

Michelle L. Verbsky ◽

Tara L. Robertson ◽

John C. Larkin ◽

Barbara N. Kunkel

Keyword(s):

Gene Expression ◽

Arabidopsis Thaliana ◽

Resistance Gene ◽

Pseudomonas Syringae ◽

Bacterial Pathogen ◽

Defense Responses ◽

Negative Regulator ◽

Suppressor Mutations ◽

Defense Related Gene ◽

Rapid Activation

In resistant plants, pathogen attack often leads to rapid activation of defense responses that limit multiplication and spread of the pathogen. To investigate the signaling mechanisms underlying this process, we carried out a screen for mutants in the signaling pathway governing resistance in Arabidopsis thaliana to the bacterial pathogen Pseudomonas syringae. This involved screening for suppressor mutations that restored resistance to a susceptible line carrying a mutation in the RPS2 resistance gene. A mutant that conferred resistance by activating defense responses in the absence of pathogens was isolated. This mutant, which carries a mutation at the CPR5 locus and was thus designated cpr5-2, exhibited resistance to P. syringae, spontaneous development of necrotic lesions, elevated PR gene expression in the absence of pathogens, and abnormal trichomes. Resistance gene-mediated defenses, including the hypersensitive response, restriction of pathogen growth, and induction of defense-related gene expression, were functional in cpr5-2 mutant plants. Additionally, in cpr5-2 plants RPS2-mediated induction of PR-1 expression was enhanced, whereas RPM1-mediated induction of ELI3 was not. These findings suggest that CPR5 encodes a negative regulator of the RPS2 signal transduc-tion pathway.

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MicroRNA844-Guided Downregulation of Cytidinephosphate Diacylglycerol Synthase3 (CDS3) mRNA Affects the Response of Arabidopsis thaliana to Bacteria and Fungi

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-02-15-0028-r ◽

2015 ◽

Vol 28 (8) ◽

pp. 892-900 ◽

Cited By ~ 7

Author(s):

Hwa Jung Lee ◽

Young Ju Park ◽

Kyung Jin Kwak ◽

Donghyun Kim ◽

June Hyun Park ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Pseudomonas Syringae ◽

Defense Response ◽

Cleavage Site ◽

Severe Disease ◽

Mrna Level ◽

Transcript Level ◽

Loss Of Function ◽

Pathogen Challenge ◽

Bacteria And Fungi

Despite the fact that a large number of miRNA sequences have been determined in diverse plant species, reports demonstrating the functional roles of miRNAs in the plant response to pathogens are severely limited. Here, Arabidopsis thaliana miRNA844 (miR844) was investigated for its functional role in the defense response to diverse pathogens. Transgenic Arabidopsis plants overexpressing miR844 (35S::miR844) displayed much more severe disease symptoms than the wild-type plants when challenged with the bacterium Pseudomonas syringae pv. tomato DC3000 or the fungus Botrytis cinerea. By contrast, a loss-of-function mir844 mutant showed an enhanced resistance against the pathogens. Although no cleavage was observed at the predicted cleavage site of the putative target mRNA, cytidinephosphate diacylglycerol synthase3 (CDS3), cleavage was observed at 6, 12, 21, or 52 bases upstream of the predicted cleavage site of CDS3 mRNA, and the level of CDS3 mRNA was downregulated by the overexpression of miR844, implying that miR844 influences CDS3 transcript level. To further confirm that the miR844-mediated defense response was due to the decrease in CDS3 mRNA level, the disease response of a CDS3 loss-of-function mutant was analyzed upon pathogen challenge. Increased susceptibility of both cds3 mutant and 35S::miR844 plants to pathogens confirmed that miR844 affected the defense response by downregulating CDS3 mRNA. The expression of miR844 was decreased, and the CDS3 transcript level increased upon pathogen challenge. Taken together, these results provide evidence that downregulation of miR844 and a concomitant increase in CDS3 expression is a defensive response of Arabidopsis to bacteria and fungi.

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Loss of function of bHLH transcription factor Nrd1 in tomato induces an arabinogalactan protein-encoding gene and enhances resistance to Pseudomonas syringae pv. tomato

10.1101/2021.11.08.467746 ◽

2021 ◽

Author(s):

Ning Zhang ◽

Chloe Hecht ◽

Xuepeng Sun ◽

Zhangjun Fei ◽

Gregory B Martin

Keyword(s):

Transcription Factor ◽

Pseudomonas Syringae ◽

Transcript Abundance ◽

Negative Regulator ◽

Arabinogalactan Protein ◽

Bhlh Transcription Factor ◽

Dependent Manner ◽

Rna Seq ◽

Loss Of Function ◽

Encoding Gene

Basic helix-loop-helix (bHLH) transcription factors constitute a superfamily in eukaryotes but their roles in plant immunity remain largely uncharacterized. We found that the transcript abundance in tomato leaves of one bHLH transcription factor-encoding gene, Nrd1 (negative regulator of resistance to DC3000 1), was significantly increased after treatment with the immunity-inducing flgII-28 peptide. Plants carrying a loss-of-function mutation in Nrd1 (Δnrd1) showed enhanced resistance to Pseudomonas syringae pv. tomato (Pst) DC3000 although early pattern-triggered immunity responses such as generation of reactive oxygen species and activation of mitogen-activated protein kinases after treatment with flagellin-derived flg22 and flgII-28 peptides were unaltered compared to wild-type plants. An RNA-Seq analysis identified a gene, Agp1, whose expression is strongly suppressed in an Nrd1-dependent manner. Agp1 encodes an arabinogalactan protein and overexpression of the Agp1 gene in Nicotiana benthamiana led to ~10-fold less Pst growth compared to the control. These results suggest that the Nrd1 protein promotes tomato susceptibility to Pst by suppressing the defense gene Agp1. RNA-Seq also revealed that loss of Nrd1 function has no effect on the transcript abundance of immunity-associated genes including Bti9, Core, Fls2, Fls3 and Wak1 upon Pst inoculation, suggesting that the enhanced immunity observed in the Δnrd1 mutants is due to the activation of key PRR signaling components as well as loss of Nrd1-regulated suppression of Agp1.

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Perturbations of a Kinase-Pseudokinase Module Activate Plant Immunity

10.1101/531665 ◽

2019 ◽

Author(s):

D. Patrick Bastedo ◽

Derek Seto ◽

Alexandre Martel ◽

Madiha Khan ◽

Inga Kireeva ◽

...

Keyword(s):

Immune Response ◽

Arabidopsis Thaliana ◽

Immune Responses ◽

Pseudomonas Syringae ◽

Molecular Mechanisms ◽

Kinase Domain ◽

Host Cells ◽

In Planta ◽

Plant Host ◽

Model Plant

ABSTRACTThe Pseudomonas syringae acetyltransferase HopZ1a is delivered directly into host cells by the type III secretion system to promote bacterial growth. However, in the model plant host Arabidopsis thaliana, HopZ1a activity results in an effector-triggered immune response (ETI) that limits bacterial proliferation. HopZ1a-triggered immunity requires the nucleotide-binding, leucine-rich repeat domain (NLR) protein, ZAR1, and the ZED1 pseudokinase. Here we demonstrate that HopZ1a can acetylate members of a family of ‘receptor-like cytoplasmic kinases’ (RLCK family VII; also known as PBS1-like kinases, or PBLs) and promote their interaction with ZED1 and ZAR1 to form a ZAR1/ZED1/PBL ternary complex. Interactions between ZED1 and PBL kinases are determined by the pseudokinase features of ZED1, and mutants designed to restore ZED1 kinase motifs can (1) bind to PBLs, (2) recruit ZAR1, and (3) trigger immunity in planta, all independently of HopZ1a. Our results suggest that interactions between these two RLCK families are promoted by perturbations of structural features that distinguish active from inactive kinase domain conformations. We propose that effector-induced interactions between ZED1/ZRK pseudokinases (RLCK family XII) and PBL kinases (RLCK family VII) provide a sensitive mechanism for detecting perturbations of either kinase family and activating ZAR1-mediated ETI.AUTHOR SUMMARYAll plants must ward off potentially infectious microbes, and those grown in large-scale crop operations are especially vulnerable to the rapid spread of disease by successful pathogens. Although many bacteria and fungi can supress plant immune responses by producing specialized virulence proteins called ‘effectors’, these effectors can also trigger immune responses that render plants resistant to infection. We studied the molecular mechanisms underlying one such effector-triggered immune response elicited by the bacterial effector HopZ1a in the model plant host Arabidopsis thaliana. We have shown that HopZ1a promotes binding between a ZED1, a ‘pseudokinase’ required for HopZ1a-triggered immunity, and several ‘true kinases’ (known as PBLs) that are likely targets of HopZ1a activity in planta. HopZ1a-induced ZED1-PBL interactions also recruit ZAR1, an Arabidopsis ‘resistance protein’ previously implicated in HopZ1a-triggered immunity. Importantly, ZED1 mutants that restore degenerate kinase motifs can bridge interactions between PBLs and ZAR1 (independently of HopZ1a) and trigger immunity in planta. Our results suggest that equilibria between active and inactive kinase domain conformations regulate ZED1-PBL interactions and formation of ternary complexes with ZAR1. Improved models describing molecular interactions between immunity determinants, effectors and effector targets will inform efforts to exploit natural diversity for development of crops with enhanced disease resistance.

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The Mechanosensitive Ion Channel MSL10 Modulates Susceptibility to Pseudomonas syringae in Arabidopsis thaliana

10.1101/2021.08.18.456837 ◽

2021 ◽

Author(s):

Debarati Basu ◽

Jennette M. Codjoe ◽

Kira Veley ◽

Elizabeth Haswell

Keyword(s):

Arabidopsis Thaliana ◽

Cell Death ◽

Ion Channel ◽

Pseudomonas Syringae ◽

Stomatal Closure ◽

Avirulence Genes ◽

Loss Of Function ◽

Susceptibility To Infection ◽

Mechanical Signals ◽

Mechanosensitive Ion Channel

Plants sense and respond to molecular signals associated with the presence of pathogens and their virulence factors. Mechanical signals generated during pathogenic invasion may also be important, but their contributions have rarely been studied. Here we investigate the potential role of a mechanosensitive ion channel, MscS-Like (MSL)10, in defense against the bacterial pathogen Pseudomonas syringae in Arabidopsis thaliana. We previously showed that overexpression of MSL10-GFP, phospho-mimetic versions of MSL10, and the gain-of-function allele msl10-3G all produce dwarfing, spontaneous cell death, and the hyperaccumulation of reactive oxygen species. These phenotypes are shared by many autoimmune mutants and are frequently suppressed by growth at high temperature in those lines. Here, we found that the same was true for all three MSL10 hypermorphs. In addition, we show that the SGT1/RAR1/HSP90 co-chaperone complex was required for dwarfing and ectopic cell death, PAD4 and SID2 were partially required, and the immune regulators EDS1 and NDR1 were dispensable. All MSL10 hypermorphs exhibited reduced susceptibility to infection by P. syringae strain Pto DC3000, Pto DC3000 expressing the avirulence genes avrRpt2 or avrRpm1, but not Pto DC3000 hrpL, and showed an accelerated induction of PR1 expression compared to wild-type plants. Null msl10-1 mutants were delayed in PR1 induction and displayed modest susceptibility to infection by COR-deficient Pst. Finally, stomatal closure was reduced in msl10-1 loss-of-function mutants in response to Pst COR−. These data show that MSL10 modulates pathogen responses and begin to address the possibility that mechanical signals are exploited by the plant for pathogen perception.

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Contrasting functions of Arabidopsis SUMO1/2 isoforms with SUMO3 intersect to modulate innate immunity and global SUMOylome responses

10.1101/2020.05.15.097535 ◽

2020 ◽

Author(s):

Kishor Dnyaneshwar Ingole ◽

Mritunjay Kasera ◽

Harrold A. van den Burg ◽

Saikat Bhattacharjee

Keyword(s):

Arabidopsis Thaliana ◽

Steady State ◽

Heat Shock ◽

Pseudomonas Syringae ◽

Bacterial Pathogen ◽

Defense Responses ◽

Vital Role ◽

Covalent Attachment ◽

Developmental Defects ◽

Small Proteins

AbstractReversible covalent attachment of SMALL UBIQUITIN-LIKE MODIFIERS (SUMOs) on target proteins regulate diverse cellular process across all eukaryotes. In Arabidopsis thaliana, most mutants with perturbed global SUMOylome display severe impairments in growth and adaptations to physiological stresses. Since SUMOs self-regulate activities of SUMOylation-associated proteins, existence of multiple isoforms introduces possibilities of their functional intersections which remain unexplored especially in plant systems. Using well-established defense responses elicited against virulent and avirulent Pseudomonas syringae pv. tomato strains, we investigated crosstalks in individual and combinatorial Arabidopsis sum mutants. Here we report that while SUM1 and SUM2 additively, but not equivalently suppress basal and TNL-specific immunity via down-regulation of salicylic acid (SA)-dependent responses, SUM3 promotes these defenses genetically downstream of SA. Remarkably, the expression of SUM3 is transcriptionally suppressed by SUMO1 or SUMO2. The loss of SUM3 not only lowers basal or post-bacterial challenge responsive enhancements of SUMO1/2-congugates but also reduces upregulation dynamics of defensive proteins and SUMOylation-associated transcripts. Combining a sum3 mutation partially attenuates heightened immunity of sum1 or sum2 mutants suggesting intricate functional impingements among these isoforms in optimizing immune amplitudes. Similar SUM1-SUM3 intersections also affect global SUMOylome responses to heat-shock affecting most notably the induction of selective heat-shock transcription factors. Overall, our investigations reveal novel insights into auto-regulatory mechanisms among SUMO isoforms in host SUMOylome maintenance and adjustments to environmental challenges.Author SummaryIn plants, similar to animals, protein functions are regulated at multiple levels. One prevalent mode is to allow covalent linkage of small proteins to specific amino acids on targets thereby affecting its fate and function. One such kind of modification named as SUMOylation involves attachment of SUMO proteins. A plant maintains strict control over its pool of SUMOylated proteins (termed SUMOylome) which upon biotic or abiotic stresses are altered to facilitate appropriate responses, returning back to steady-state when the threat subsides. In mutants of the model plant Arabidopsis thaliana having disturbed steady-state SUMOylome, growth and developmental defects ensue. These mutants are auto-immune showing more resistance to infection by the bacterial pathogen Pseudomonas syringae. However, Arabidopsis SUMO-family are comprised of multiple members raising the question about their specificity or functional crosstalks. We discovered that two SUMO members function in coordination to suppress immunity including the repression of a third member which supports defenses. The expression of this third member during pathogen attack or heat-shock influences the responsive changes in the host SUMOylome likely suggesting SUMOs themselves play vital role in these adaptations. Overall, our work highlights novel intersections of SUMO members in mounting stress-specific responses.

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The IMMUNE-ASSOCIATED NUCLEOTIDE-BINDING 9 protein is a regulator of basal immunity in Arabidopsis thaliana

10.1101/277269 ◽

2018 ◽

Author(s):

Yuanzheng Wang ◽

Yansha Li ◽

Tabata Rosas-Diaz ◽

Carlos Caceres-Moreno ◽

Rosa Lozano-Duran ◽

...

Keyword(s):

Immune Responses ◽

Pseudomonas Syringae ◽

Expression Patterns ◽

Nucleotide Binding ◽

Negative Regulator ◽

Mass Spectrometry Analysis ◽

Crop Species ◽

Spectrometry Analysis ◽

Basal Immunity

AbstractA robust regulation of plant immune responses requires multitude of positive and negative regulators that act in concert. The immune-associated nucleotide-binding (IAN) gene family members are associated with immunity in different organisms, although no characterization of their function has been carried out to date in plants. In this work, we analyzed the expression patterns of IAN genes and found that IAN9 is repressed upon pathogen infection or treatment with immune elicitors. IAN9 encodes a plasma membrane-localized protein that genetically behaves as a negative regulator of immunity. A novel ian9 mutant generated by CRISPR/Cas9 shows increased resistance to Pseudomonas syringae, while transgenic plants overexpressing IAN9 show a slight increase in susceptibility. In vivo immunoprecipitation of IAN9-GFP followed by mass spectrometry analysis revealed that IAN9 associates with a previously uncharacterized C3HC4-type RING finger domain-containing protein that we named IAP1, for IAN9-associated protein 1, which also acts as a negative regulator of basal immunity. Interestingly, neither ian9 or iap1 mutant plants show any obvious developmental phenotype, suggesting that they display enhanced inducible immunity rather than constitutive immune responses. Since both IAN9 and IAP1 have orthologs in important crop species, they could be suitable targets to generate plants more resistant to diseases caused by bacterial pathogens without yield penalty.

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Mqo, a Tricarboxylic Acid Cycle Enzyme, Is Required for Virulence of Pseudomonas syringae pv. tomato Strain DC3000 on Arabidopsis thaliana

Journal of Bacteriology ◽

10.1128/jb.01570-08 ◽

2009 ◽

Vol 191 (9) ◽

pp. 3132-3141 ◽

Cited By ~ 19

Author(s):

Eve M. Mellgren ◽

Andrew P. Kloek ◽

Barbara N. Kunkel

Keyword(s):

Arabidopsis Thaliana ◽

Pseudomonas Syringae ◽

Virulence Factors ◽

Plant Tissue ◽

Pathogenic Bacteria ◽

Tricarboxylic Acid Cycle ◽

Tricarboxylic Acid ◽

Wild Type ◽

In Planta ◽

Acid Cycle

ABSTRACT Plant pathogenic bacteria, such as Pseudomonas syringae pv. tomato strain DC3000, the causative agent of tomato bacterial speck disease, grow to high levels in the apoplastic space between plant cells. Colonization of plant tissue requires expression of virulence factors that modify the apoplast to make it more suitable for pathogen growth or facilitate adaptation of the bacteria to the apoplastic environment. To identify new virulence factors involved in these processes, DC3000 Tn5 transposon insertion mutants with reduced virulence on Arabidopsis thaliana were identified. In one of these mutants, the Tn5 insertion disrupted the malate:quinone oxidoreductase gene (mqo), which encodes an enzyme of the tricarboxylic acid cycle. mqo mutants do not grow to wild-type levels in plant tissue at early time points during infection. Further, plants infected with mqo mutants develop significantly reduced disease symptoms, even when the growth of the mqo mutant reaches wild-type levels at late stages of infection. Mutants lacking mqo function grow more slowly in culture than wild-type bacteria when dicarboxylates are the only available carbon source. To explore whether dicarboxylates are important for growth of DC3000 in the apoplast, we disrupted the dctA1 dicarboxylate transporter gene. DC3000 mutants lacking dctA1 do not grow to wild-type levels in planta, indicating that transport and utilization of dicarboxylates are important for virulence of DC3000. Thus, mqo may be required by DC3000 to meet nutritional requirements in the apoplast and may provide insight into the mechanisms underlying the important, but poorly understood process of adaptation to the host environment.

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