scholarly journals Transcriptome landscape of a bacterial pathogen under plant immunity

2018 ◽  
Vol 115 (13) ◽  
pp. E3055-E3064 ◽  
Author(s):  
Tatsuya Nobori ◽  
André C. Velásquez ◽  
Jingni Wu ◽  
Brian H. Kvitko ◽  
James M. Kremer ◽  
...  
Keyword(s):  
Immune Response ◽  
Pseudomonas Syringae ◽  
Bacterial Growth ◽  
Plant Pathogens ◽  
Plant Immunity ◽  
Expression Patterns ◽  
Bacterial Pathogen ◽  
In Planta ◽  
Bacterial Strains ◽  
Bacterial Genes

Plant pathogens can cause serious diseases that impact global agriculture. The plant innate immunity, when fully activated, can halt pathogen growth in plants. Despite extensive studies into the molecular and genetic bases of plant immunity against pathogens, the influence of plant immunity in global pathogen metabolism to restrict pathogen growth is poorly understood. Here, we developed RNA sequencing pipelines for analyzing bacterial transcriptomes in planta and determined high-resolution transcriptome patterns of the foliar bacterial pathogen Pseudomonas syringae in Arabidopsis thaliana with a total of 27 combinations of plant immunity mutants and bacterial strains. Bacterial transcriptomes were analyzed at 6 h post infection to capture early effects of plant immunity on bacterial processes and to avoid secondary effects caused by different bacterial population densities in planta. We identified specific “immune-responsive” bacterial genes and processes, including those that are activated in susceptible plants and suppressed by plant immune activation. Expression patterns of immune-responsive bacterial genes at the early time point were tightly linked to later bacterial growth levels in different host genotypes. Moreover, we found that a bacterial iron acquisition pathway is commonly suppressed by multiple plant immune-signaling pathways. Overexpression of a P. syringae sigma factor gene involved in iron regulation and other processes partially countered bacterial growth restriction during the plant immune response triggered by AvrRpt2. Collectively, this study defines the effects of plant immunity on the transcriptome of a bacterial pathogen and sheds light on the enigmatic mechanisms of bacterial growth inhibition during the plant immune response.

scholarly journals In planta bacterial multi-omics analysis illuminates regulatory principles underlying plant-pathogen interactions

2019 ◽  
Author(s):  
Tatsuya Nobori ◽  
Yiming Wang ◽  
Jingni Wu ◽  
Sara Christina Stolze ◽  
Yayoi Tsuda ◽  
...  
Keyword(s):  
Gene Regulation ◽  
Pseudomonas Syringae ◽  
Protein Level ◽  
Plant Pathogens ◽  
Plant Immunity ◽  
Bacterial Pathogen ◽  
Bacterial Virulence ◽  
In Planta ◽  
Bacterial Gene ◽  
Global Food Security

AbstractUnderstanding how gene expression is regulated in plant pathogens is crucial for pest control and thus global food security. An integrated understanding of bacterial gene regulation in the host is dependent on multi-omic datasets, but these are largely lacking. Here, we simultaneously characterized the transcriptome and proteome of a foliar bacterial pathogen, Pseudomonas syringae, in Arabidopsis thaliana and identified a number of bacterial processes influenced by plant immunity at the mRNA and the protein level. We found instances of both concordant and discordant regulation of bacterial mRNAs and proteins. Notably, the tip component of bacterial type III secretion system was selectively suppressed by the plant salicylic acid pathway at the protein level, suggesting protein-level targeting of the bacterial virulence system by plant immunity. Furthermore, gene co-expression analysis illuminated previously unknown gene regulatory modules underlying bacterial virulence and their regulatory hierarchy. Collectively, the integrated in planta bacterial omics approach provides molecular insights into multiple layers of bacterial gene regulation that contribute to bacterial growth in planta and elucidate the role of plant immunity in controlling pathogens.

scholarly journals AlgU, a conserved sigma factor regulating abiotic stress tolerance and promoting virulence in Pseudomonas syringae.

2020 ◽  
Author(s):  
Haibi Wang ◽  
Zichu Yang ◽  
Bryan Swingle ◽  
Brian H Kvitko
Keyword(s):  
Pseudomonas Syringae ◽  
Sigma Factor ◽  
Plant Pathogens ◽  
Plant Immunity ◽  
Abiotic Stress Tolerance ◽  
Expression Patterns ◽  
Environmental Signals ◽  
Bacterial Physiology ◽  
Biotic Stresses ◽  
Activation Mechanisms

Pseudomonas syringae can rapidly deploy specialized functions to deal with abiotic and biotic stresses. Host niches pose specific sets of environmental challenges driven in part by immune defenses. Bacteria use a “just-in-time” strategy of gene regulation, meaning that they only produce the functions necessary for survival as needed. Extracytoplasmic function (ECF) sigma factors transduce a specific set of environmental signals and change gene expression patterns by altering RNAP promoter specificity, to adjust bacterial physiology, structure, and/or behavior to improve chances of survival. The broadly conserved ECF sigma factor, AlgU, affects virulence in both animal and plant pathogens. Pseudomonas syringae AlgU controls expression of more than 800 genes, some of which contribute to suppression of plant immunity and bacterial fitness in plants. This review discusses AlgU activation mechanisms, functions controlled by AlgU, and how these functions contribute to P. syringae survival in plants.

scholarly journals Dual Role of Auxin in Regulating Plant Defense and Bacterial Virulence Gene Expression During Pseudomonas syringae PtoDC3000 Pathogenesis

2020 ◽  
Vol 33 (8) ◽  
pp. 1059-1071 ◽  
Author(s):  
Arnaud T. Djami-Tchatchou ◽  
Gregory A. Harrison ◽  
Chris P. Harper ◽  
Renhou Wang ◽  
Michael J. Prigge ◽  
...  
Keyword(s):  
Gene Expression ◽  
Pseudomonas Syringae ◽  
Bacterial Growth ◽  
Plant Pathogens ◽  
Virulence Gene ◽  
Bacterial Virulence ◽  
Auxin Signaling ◽  
Host Defenses ◽  
In Planta ◽  
Virulence Gene Expression

Modification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen strain Pseudomonas syringae DC3000 (PtoDC3000) produces the plant hormone auxin (indole-3-acetic acid [IAA]) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth and that this phenotype was suppressed by introducing the sid2-2 mutation, which impairs SA synthesis. Thus, host auxin signaling is required for normal susceptibility to PtoDC3000 and is involved in suppressing SA-mediated defenses. Unexpectedly, tir1 afb1 afb4 afb5 quadruple-mutant plants lacking four of the six known auxin coreceptors that exhibit decreased auxin perception, supported increased levels of bacterial growth. This mutant exhibited elevated IAA levels and reduced SA-mediated defenses, providing additional evidence that auxin promotes disease by suppressing host defense. We also investigated the hypothesis that IAA promotes PtoDC3000 virulence through a direct effect on the pathogen and found that IAA modulates expression of virulence genes, both in culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.

scholarly journals Dual role of auxin in regulating plant defense and bacterial virulence gene expression during Pseudomonas syringae PtoDC3000 pathogenesis

2019 ◽  
Author(s):  
Arnaud T. Djami-Tchatchou ◽  
Gregory A. Harrison ◽  
Chris P. Harper ◽  
Renhou Wang ◽  
Michael J. Prigge ◽  
...  
Keyword(s):  
Gene Expression ◽  
Pseudomonas Syringae ◽  
Bacterial Growth ◽  
Plant Pathogens ◽  
Virulence Gene ◽  
Bacterial Virulence ◽  
Auxin Signaling ◽  
Host Defenses ◽  
In Planta ◽  
Virulence Gene Expression

ABSTRACTModification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen Pseudomonas syringae strain PtoDC3000 produces the plant hormone auxin (Indole-3-acetic acid, or IAA) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth, demonstrating that host auxin signaling is required for normal susceptibility to PtoDC3000, and this phenotype was dependent on SA-mediated defenses. However, despite exhibiting decreased auxin perception, tir1 afb1 afb4 afb5 quadruple mutant plants lacking four of the six known auxin co-receptors supported increased levels of bacterial growth. This mutant also exhibited elevated IAA levels, suggesting that the increased IAA in these plants may promote PtoDC3000 growth independent of host auxin signaling, perhaps through a direct effect on the pathogen. In support of this, we found that IAA directly impacted the pathogen, by modulating expression of bacterial virulence genes, both in liquid culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.

scholarly journals Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis

2020 ◽  
Vol 71 (18) ◽  
pp. 5562-5576
Author(s):  
Yi Liu ◽  
Kunru Wang ◽  
Qiang Cheng ◽  
Danyu Kong ◽  
Xunzhong Zhang ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Cysteine Protease ◽  
Plant Immunity ◽  
Stomatal Closure ◽  
Bacterial Pathogen ◽  
E3 Ligase ◽  
Biotic Stresses ◽  
Ubiquitin E3 Ligase ◽  
Induced Immunity

Abstract Plants can be simultaneously exposed to multiple stresses. The interplay of abiotic and biotic stresses may result in synergistic or antagonistic effects on plant development and health. Temporary drought stress can stimulate plant immunity; however, the molecular mechanism of drought-induced immunity is largely unknown. In this study, we demonstrate that cysteine protease RD21A is required for drought-induced immunity. Temporarily drought-treated wild-type Arabidopsis plants became more sensitive to the bacterial pathogen-associated molecular pattern flg22, triggering stomatal closure, which resulted in increased resistance to Pseudomonas syringae pv. tomato DC3000 (Pst-DC3000). Knocking out rd21a inhibited flg22-triggered stomatal closure and compromised the drought-induced immunity. Ubiquitin E3 ligase SINAT4 interacted with RD21A and promoted its degradation in vivo. The overexpression of SINAT4 also consistently compromised the drought-induced immunity to Pst-DC3000. A bacterial type III effector, AvrRxo1, interacted with both SINAT4 and RD21A, enhancing SINAT4 activity and promoting the degradation of RD21A in vivo. Therefore, RD21A could be a positive regulator of drought-induced immunity, which could be targeted by pathogen virulence effectors during pathogenesis.

scholarly journals Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns

2015 ◽  
Vol 112 (17) ◽  
pp. 5533-5538 ◽  
Author(s):  
Manuel Benedetti ◽  
Daniela Pontiggia ◽  
Sara Raggi ◽  
Zhenyu Cheng ◽  
Flavio Scaloni ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Immunity ◽  
Inducible Promoter ◽  
Spectrometric Analysis ◽  
In Planta ◽  
Gene Encoding ◽  
Polygalacturonase Inhibiting Protein ◽  
Molecular Patterns ◽  
Damage Associated Molecular Patterns

Oligogalacturonides (OGs) are fragments of pectin that activate plant innate immunity by functioning as damage-associated molecular patterns (DAMPs). We set out to test the hypothesis that OGs are generated in planta by partial inhibition of pathogen-encoded polygalacturonases (PGs). A gene encoding a fungal PG was fused with a gene encoding a plant polygalacturonase-inhibiting protein (PGIP) and expressed in transgenic Arabidopsis plants. We show that expression of the PGIP–PG chimera results in the in vivo production of OGs that can be detected by mass spectrometric analysis. Transgenic plants expressing the chimera under control of a pathogen-inducible promoter are more resistant to the phytopathogens Botrytis cinerea, Pectobacterium carotovorum, and Pseudomonas syringae. These data provide strong evidence for the hypothesis that OGs released in vivo act as a DAMP signal to trigger plant immunity and suggest that controlled release of these molecules upon infection may be a valuable tool to protect plants against infectious diseases. On the other hand, elevated levels of expression of the chimera cause the accumulation of salicylic acid, reduced growth, and eventually lead to plant death, consistent with the current notion that trade-off occurs between growth and defense.

scholarly journals Identification of Loci of Pseudomonas syringae pv. actinidiae Involved in Lipolytic Activity and Their Role in Colonization of Kiwifruit Leaves

2017 ◽  
Vol 107 (6) ◽  
pp. 645-653 ◽  
Author(s):  
Hitendra Kumar Patel ◽  
Patrizia Ferrante ◽  
Meng Xianfa ◽  
Sree Gowrinadh Javvadi ◽  
Sujatha Subramoni ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Pathogens ◽  
Lipid A ◽  
Lipolytic Activity ◽  
Genetic Screen ◽  
Economic Losses ◽  
In Planta ◽  
Tn5 Transposon ◽  
Tn5 Mutants ◽  
Transposon Mutants

Bacterial canker disease caused by Pseudomonas syringae pv. actinidiae, an emerging pathogen of kiwifruit plants, has recently brought about major economic losses worldwide. Genetic studies on virulence functions of P. syringae pv. actinidiae have not yet been reported and there is little experimental data regarding bacterial genes involved in pathogenesis. In this study, we performed a genetic screen in order to identify transposon mutants altered in the lipolytic activity because it is known that mechanisms of regulation, production, and secretion of enzymes often play crucial roles in virulence of plant pathogens. We aimed to identify the set of secretion and global regulatory loci that control lipolytic activity and also play important roles in in planta fitness. Our screen for altered lipolytic activity phenotype identified a total of 58 Tn5 transposon mutants. Mapping all these Tn5 mutants revealed that the transposons were inserted in genes that play roles in cell division, chemotaxis, metabolism, movement, recombination, regulation, signal transduction, and transport as well as a few unknown functions. Several of these identified P. syringae pv. actinidiae Tn5 mutants, notably the functions affected in phosphomannomutase AlgC, lipid A biosynthesis acyltransferase, glutamate–cysteine ligase, and the type IV pilus protein PilI, were also found affected in in planta survival and/or growth in kiwifruit plants. The results of the genetic screen and identification of novel loci involved in in planta fitness of P. syringae pv. actinidiae are presented and discussed.

The 73-kb pIAA plasmid increases competitive fitness of Pseudomonas syringae subspecies savastanoi in oleander

1993 ◽  
Vol 39 (7) ◽  
pp. 659-664 ◽  
Author(s):  
Sara E. Silverstone ◽  
David G. Gilchrist ◽  
Richard M. Bostock ◽  
Tsune Kosuge
Keyword(s):  
Population Density ◽  
Pseudomonas Syringae ◽  
Indoleacetic Acid ◽  
Leaf Tissue ◽  
Insertion Mutant ◽  
Wild Type ◽  
In Planta ◽  
Bacterial Strains ◽  
Growth And Survival ◽  
Iaa Production

Pseudomonas syringae subsp. savastanoi causes tumors on olive and oleander by producing the plant growth regulators indoleacetic acid (IAA) and cytokinins following infection of the plant. The contribution of IAA production to the ability of P. syringae subsp. savastanoi to grow and survive in oleander leaf tissue was studied. Bacterial strains differing only with respect to IAA production were characterized. Growth and survival of wild-type and two mutant strains of P. syringae subsp. savastanoi in oleander leaf tissue were monitored by weekly colony counts and IAA plate assays. Growth rate of the three strains in culture and in planta did not differ significantly. However, the wild-type strain reached a higher population density and maintained its maximum density at least 9 weeks longer than either mutant population. An insertion mutant containing the IAA plasmid (pIAA), but incapable of IAA production, did not maintain a higher population density than a strain cured of the IAA plasmid. The pIAA-cured strain maintained a higher population density when coinoculated with an IAA-producing strain than when inoculated alone. These results suggest that IAA production may contribute to the fitness of P. syringae subsp. savastanoi in oleander tissue and that the iaa operon alone may be responsible for the competitive advantage of cells harboring pIAA.Key words: indoleacetic acid, bacterial ecology.

scholarly journals Relationship of Genes Conferring Epiphytic Fitness and Internal Multiplication in Plants in Erwinia herbicola

2000 ◽  
Author(s):  
Steven Lindow ◽  
Isaac Barash ◽  
Shulamit Manulis
Keyword(s):  
Plant Pathogens ◽  
Regulatory Control ◽  
Virulence Determinants ◽  
Plant Interactions ◽  
In Planta ◽  
Cytokinin Biosynthesis ◽  
Erwinia Herbicola ◽  
Phytopathogenic Bacterium ◽  
Plant Environment ◽  
Bacterial Genes

Most bacterial plant pathogens colonize the surface of healthy plants as epiphytes before colonizing internally and initiating disease. The epiphytic phase of these pathogens is thus an important aspect of their epidemiology and a stage at which chemical and biological control is aimed. However, little is known of the genes and phenotypes that contribute to the ability of bacteria to grow on leaves and survive the variable physical environment in this habitat. In addition, while genes such as hrp awr and others which confer pathogenicity and in planta growth ability have been described, their contribution to other aspects of bacterial epidemiology such as epiphytic fitness have not been addressed. We hypothesized that bacterial genes conferring virulence or pathogenicity to plants also contribute to the epiphytic fitness of these bacteria and that many of these genes are preferentially located on plasmids. We addressed these hypotheses by independently identifying genes that contribute to epiphytic fitness, in planta growth, virulence and pathogenicity in the phytopathogenic bacterium Erwinia herbicola pv gypsophilae which causes gall formation on gypsophila. This species is highly epiphytically fit and has acquired a plasmid (pPATH) that contains numerous pathogenicity and virulence determinants, which we have found to also contribute to epiphytic fitness. We performed saturation transposon mutagenesis on pPATH as well as of the chromosome of E.h. gypsophilae, and identified mutants with reduced ability to grow in plants and/or cause disease symptoms, and through a novel competition assay, identified mutants less able to grow or survive on leaves. The number and identity of plasmid-borne hrp genes required for virulence was determined from an analysis of pPATH mutants, and the functional role of these genes in virulence was demonstrated. Likewise, other pPATH-encoded genes involved in IAA and cytokinin biosynthesis were characterized and their pattern of transcriptional activity was determined in planta. In both cases these genes involved in virulence were found to be induced in plant apoplasts. About half of avirulent mutants in pPATH were also epiphytically unfit whereas only about 10% of chromosomal mutants that were avirulent also had reduced epiphytic fitness. About 18% of random mutants in pPATH were avirulent in contrast to only 2.5% of random chromosomal mutants. Importantly, as many as 28% of pPATH mutants had lower epiphytic fitness while only about 10% of random chromosomal mutants had lower epiphytic fitness. These results support both of our original hypotheses, and indicate that genes important in a variety of interactions with plant have been enriched on mobile plasmids such as pPATH. The results also suggest that the ability of bacteria to colonize the surface of plants and to initiate infections in the interior of plants involves many of the same traits. These traits also appear to be under strong regulatory control, being expressed in response to the plant environment in many cases. It may be possible to alter the pattern of expression of such genes by altering the chemical environment of plants either by genetic means or by additional or chemical antagonists of the plant signals. The many novel bacterial genes identified in this study that are involved in plant interactions should be useful in further understanding of bacterial plant interactions.

scholarly journals The ecological genetics ofPseudomonas syringaefrom kiwifruit leaves

2017 ◽  
Author(s):  
Christina Straub ◽  
Elena Colombi ◽  
Li Li ◽  
Hongwen Huang ◽  
Matthew D. Templeton ◽  
...  
Keyword(s):  
Population Structure ◽  
Pseudomonas Syringae ◽  
Bacterial Pathogen ◽  
Ecological Factors ◽  
Ecological Genetics ◽  
Plant Interactions ◽  
In Planta ◽  
Canker Disease ◽  
Pathogen Populations

SUMMARYInteractions between commensal microbes and invading pathogens are understudied, despite their likely effects on pathogen population structure and infection processes. We describe the population structure and genetic diversity of a broad range of co-occurringPseudomonas syringaeisolated from infected and uninfected kiwifruit during an outbreak of bleeding canker disease caused byP. syringaepv.actinidiae(Psa) in New Zealand. Overall population structure was clonal and affected by ecological factors including infection status and cultivar. Most isolates are members of a new clade in phylogroup 3 (PG3a), also present on kiwifruit leaves in China and Japan. Stability of the polymorphism between pathogenicPsaand commensalP. syringaePG3a isolated from the same leaf was tested using reciprocal invasion from rare assaysin vitroand in planta.P. syringaeG33C (PG3a) inhibitedPsaNZ54, while the presence ofPsaNZ54 enhanced the growth ofP. syringaeG33C. This effect could not be attributed to virulence activity encoded by the Type 3 secretion system ofPsa. Together our data contribute toward the development of an ecological perspective on the genetic structure of pathogen populations.ORIGINALITY-SIGNIFICANT STATEMENTBacterial pathogen populations are often studied with little consideration of co-occurring microbes and yet interactions between pathogens and commensals can affect both population structure and disease progression. A fine-scale sampling of commensals present on kiwifruit leaves during an outbreak of bleeding canker disease caused byP. syringaepv.actinidiaereveals a clonal population structure. A new clade of non-pathogenicP. syringae(PG3a) appears to be associated with kiwifruit on a global scale. The presence of PG3a on kiwifruit has significant effects on the outcome of infection byP. syringaepv.actinidiae. This emphasises the value of studying the effect of co-occurring bacteria on pathogen-plant interactions.

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