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The flagella of ‘ Candidatus Liberibacter asiaticus’ and its movement in planta

Journal Article · · Molecular Plant Pathology
DOI:https://doi.org/10.1111/mpp.12884· OSTI ID:1574057
 [1];  [1];  [1];  [1];  [2];  [3];  [1]
  1. Citrus Research and Education Center Department of Microbiology and Cell Science University of Florida/Institute of Food and Agricultural Sciences Lake Alfred FL USA
  2. Citrus Research and Education Center Department of Microbiology and Cell Science University of Florida/Institute of Food and Agricultural Sciences Lake Alfred FL USA, National Engineering Research Center for Citrus, Citrus Research Institute, Southwest University Chongqing 400712 People’s Republic of China
  3. Emerging Pathogens Institute University of Florida Gainesville FL USA
Summary

Citrus huanglongbing (HLB) is the most devastating citrus disease worldwide. ‘ Candidatus Liberibacter asiaticus’ (Las) is the most prevalent HLB causal agent that is yet to be cultured. Here, we analysed the flagellar genes of Las and Rhizobiaceae and observed two characteristics unique to the flagellar proteins of Las: (i) a shorter primary structure of the rod capping protein FlgJ than other Rhizobiaceae bacteria and (ii) Las contains only one flagellin‐encoding gene flaA (CLIBASIA_02090), whereas other Rhizobiaceae species carry at least three flagellin‐encoding genes. Only flgJ Atu but not flgJ Las restored the swimming motility of Agrobacterium tumefaciens flgJ mutant. Pull‐down assays demonstrated that FlgJ Las interacts with FlgB but not with FliE. Ectopic expression of flaA Las in A. tumefaciens mutants restored the swimming motility of ∆ flaA mutant and ∆ flaAD mutant, but not that of the null mutant ∆ flaABCD . No flagellum was observed for Las in citrus and dodder. The expression of flagellar genes was higher in psyllids than in planta . In addition, western blotting using flagellin‐specific antibody indicates that Las expresses flagellin protein in psyllids, but not in planta . The flagellar features of Las in planta suggest that Las movement in the phloem is not mediated by flagella. We also characterized the movement of Las after psyllid transmission into young flush. Our data support a model that Las remains inside young flush after psyllid transmission and before the flush matures. The delayed movement of Las out of young flush after psyllid transmission provides opportunities for targeted treatment of young flush for HLB control.

Sponsoring Organization:
USDOE
OSTI ID:
1574057
Alternate ID(s):
OSTI ID: 1574059
Journal Information:
Molecular Plant Pathology, Journal Name: Molecular Plant Pathology Journal Issue: 1 Vol. 21; ISSN 1464-6722
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (86)

Self-assembly of the Filament Capping Protein, FliD, of Bacterial Flagella into an Annular Structure journal June 1996
The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase journal September 2001
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method journal December 2001
Domain structure of flagellin journal June 1984
The organization of the Caulobacter crescentus flagellar filament journal April 1989
Flagellin perception: a paradigm for innate immunity journal June 2002
Bacterial Flagellum: Visualizing the Complete Machine In Situ journal November 2006
Innate immune system capabilities of the Asian citrus psyllid, Diaphorina citri journal September 2017
‘Candidatus Liberibacter asiaticus’ peroxiredoxin (LasBCP) suppresses oxylipin-mediated defense signaling in citrus journal May 2019
The Citrus Huanglongbing Crisis and Potential Solutions journal May 2019
Molecular motors of the bacterial flagella journal December 2008
Sense and sensibility: flagellum-mediated gene regulation journal January 2010
Building a flagellum outside the bacterial cell journal October 2014
Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages journal April 2006
Molecular mechanisms underlying heat or tetracycline treatments for citrus HLB control journal June 2018
‘Candidatus Liberibacter asiaticus’ Accumulates inside Endoplasmic Reticulum Associated Vacuoles in the Gut Cells of Diaphorina citri journal December 2017
Liberibacter crescens biofilm formation in vitro: establishment of a model system for pathogenic ‘Candidatus Liberibacter spp.’ journal March 2019
Morphological abnormalities and cell death in the Asian citrus psyllid (Diaphorina citri) midgut associated with Candidatus Liberibacter asiaticus journal September 2016
Structure of FliM provides insight into assembly of the switch complex in the bacterial flagella motor journal August 2006
An escort mechanism for cycling of export chaperones during flagellum assembly journal November 2006
Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites journal January 2013
Asymptomatic spread of huanglongbing and implications for disease control journal June 2015
The Essential Protein for Bacterial Flagella Formation FlgJ Functions as a β- N -Acetylglucosaminidase journal September 2014
From molecular evolution to biobricks and synthetic modules: a lesson by the bacterial flagellum journal January 2014
Transmission Rates of ‘ Ca. Liberibacter asiaticus’ by Asian Citrus Psyllid Are Enhanced by the Presence and Developmental Stage of Citrus Flush journal February 2016
Enhanced Acquisition Rates of ‘ Candidatus Liberibacter asiaticus’ by the Asian Citrus Psyllid (Hemiptera: Liviidae) in the Presence of Vegetative Flush Growth in Citrus journal July 2016
Global Pattern of Gene Expression of Xanthomonas axonopodis pv. glycines Within Soybean Leaves journal June 2016
The Tad Pilus Apparatus of ‘ Candidatus Liberibacter asiaticus’ and Its Regulation by VisNR journal September 2019
The Complete Genome Sequence of ‘ Candidatus Liberibacter americanus’, Associated with Citrus Huanglongbing journal February 2014
Candidatus Liberibacter asiaticus’ Encodes a Functional Salicylic Acid (SA) Hydroxylase That Degrades SA to Suppress Plant Defenses journal August 2017
Complete Genome Sequence of Citrus Huanglongbing Bacterium, ‘ Candidatus Liberibacter asiaticus’ Obtained Through Metagenomics journal August 2009
Gene-for-Genes Interactions Between Cotton R Genes and Xanthomonas campestris pv. malvacearum avr Genes journal January 1993
A New ‘ Candidatus Liberibacter’ Species Associated with Diseases of Solanaceous Crops journal March 2009
Association of ‘ Candidatus Liberibacter solanacearum’ with Zebra Chip Disease of Potato Established by Graft and Psyllid Transmission, Electron Microscopy, and PCR journal June 2009
The in Planta Effective Concentration of Oxytetracycline Against ‘ Candidatus Liberibacter asiaticus’ for Suppression of Citrus Huanglongbing journal December 2019
Challenges for Managing Candidatus Liberibacter spp. (Huanglongbing Disease Pathogen): Current Control Measures and Future Directions journal April 2018
Field Evaluation of Plant Defense Inducers for the Control of Citrus Huanglongbing journal January 2016
Developing Citrus Huanglongbing (HLB) Management Strategies Based on the Severity of Symptoms in HLB-Endemic Citrus-Producing Regions journal April 2019
Visualization of ‘ Candidatus Liberibacter asiaticus’ Cells in the Vascular Bundle of Citrus Seed Coats with Fluorescence In Situ Hybridization and Transmission Electron Microscopy journal June 2013
Colonization of Dodder, Cuscuta indecora , by ‘ Candidatus Liberibacter asiaticus’ and ‘ Ca. L. americanus’ journal August 2010
Early Events of Citrus Greening (Huanglongbing) Disease Development at the Ultrastructural Level journal September 2010
Targeted Early Detection of Citrus Huanglongbing Causal Agent ‘ Candidatus Liberibacter asiaticus’ Before Symptom Expression journal June 2019
Citrus Huanglongbing: A Newly Relevant Disease Presents Unprecedented Challenges journal July 2013
In Planta Distribution of ‘ Candidatus Liberibacter asiaticus’ as Revealed by Polymerase Chain Reaction (PCR) and Real-Time PCR journal May 2008
Response of Sweet Orange ( Citrus sinensis ) to ‘ Candidatus Liberibacter asiaticus’ Infection: Microscopy and Microarray Analyses journal January 2009
Examination of the Responses of Different Genotypes of Citrus to Huanglongbing (Citrus Greening) Under Different Conditions journal December 2009
Agrobacterium tumefaciens possesses a fourth flagellin gene located in a large gene cluster concerned with flagellar structure, assembly and motility journal June 1999
Of PAMPs and Effectors: The Blurred PTI-ETI Dichotomy journal January 2011
The FliK protein and flagellar hook-length control journal May 2007
Control of speed modulation (chemokinesis) in the unidirectional rotary motor of Sinorhizobium meliloti : Control of chemokinesis in journal February 2005
Interaction of FliK with the bacterial flagellar hook is required for efficient export specificity switching journal October 2009
The role of the FliK molecular ruler in hook-length control in Salmonella enterica journal March 2010
Effect of plant barriers and citrus leaf age on dispersal of Diaphorina citri (Hemiptera: Liviidae) journal June 2015
Global gene expression changes in Candidatus  Liberibacter asiaticus during the transmission in distinct hosts between plant and insect : Expression profiling of journal January 2013
Exogenous N -acyl-homoserine lactones enhance the expression of flagella of Pseudomonas syringae and activate defence responses in plants : Interactions between plants and phytopathogens journal December 2016
Structural Basis of TLR5-Flagellin Recognition and Signaling journal February 2012
Infection Density Dynamics of the Citrus Greening Bacterium “Candidatus Liberibacter asiaticus” in Field Populations of the Psyllid Diaphorina citri and Its Relevance to the Efficiency of Pathogen Transmission to Citrus Plants journal March 2015
Use of a Green Fluorescent Strain for Analysis of Xylella fastidiosa Colonization of Vitis vinifera journal December 2003
AlgU Controls Expression of Virulence Genes in Pseudomonas syringae pv. tomato DC3000 journal June 2016
Antiparallel and Interlinked Control of Cellular Iron Levels by the Irr and RirA Regulators of Agrobacterium tumefaciens journal May 2011
Multiple Flagellin Proteins Have Distinct and Synergistic Roles in Agrobacterium tumefaciens Motility journal September 2018
Motility and Chemotaxis in Agrobacterium tumefaciens Surface Attachment and Biofilm Formation journal August 2007
A Single-Domain FlgJ Contributes to Flagellar Hook and Filament Formation in the Lyme Disease Spirochete Borrelia burgdorferi journal December 2011
Growth of Flagellar Filaments of Escherichia coli Is Independent of Filament Length journal March 2012
Peptidoglycan-Hydrolyzing Activity of the FlgJ Protein, Essential for Flagellar Rod Formation inSalmonella typhimurium journal March 1999
Analysis of the Polar Flagellar Gene System of Vibrio parahaemolyticus journal July 2000
Mutational Analysis of the Rhizobium lupini H13-3 and Sinorhizobium meliloti Flagellin Genes: Importance of Flagellin A for Flagellar Filament Structure and Transcriptional Regulation journal September 2001
Lateral Flagellar Gene System of Vibrio parahaemolyticus journal July 2003
MotD of Sinorhizobium meliloti and Related  -Proteobacteria Is the Flagellar-Hook-Length Regulator and Therefore Reassigned as FliK journal March 2006
Process of Protein Transport by the Type III Secretion System journal December 2004
Waveform analysis and structure of flagella and basal complexes from Bdellovibrio bacteriovorus 109J. journal January 1985
Genomic organization and expression of Campylobacter flagellin genes. journal April 1990
The Candidatus Liberibacter–Host Interface: Insights into Pathogenesis Mechanisms and Disease Control journal August 2017
How Bacteria Assemble Flagella journal October 2003
Self-Assembly and Type III Protein Export of the Bacterial Flagellum journal January 2004
Plasticity of the domain structure in FlgJ, a bacterial protein involved in flagellar rod formation journal January 2006
Two Plant Bacteria, S. meliloti and Ca. Liberibacter asiaticus, Share Functional znuABC Homologues That Encode for a High Affinity Zinc Uptake System journal May 2012
Living on the Edges: Spatial Niche Occupation of Asian Citrus Psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), in Citrus Groves journal July 2015
The Post-transcriptional Regulator rsmA/csrA Activates T3SS by Stabilizing the 5′ UTR of hrpG, the Master Regulator of hrp/hrc Genes, in Xanthomonas journal February 2014
Bacterial Flagella: Twist and Stick, or Dodge across the Kingdoms journal January 2015
Transmission Parameters for Candidatus Liberibacter asiaticus by Asian Citrus Psyllid (Hemiptera: Psyllidae) journal October 2010
Evaluation of Management Programs for Protecting Young Citrus Plantings from Huanglongbing journal March 2013
Functions of Bacterial Flagella journal January 1996
Structure, gene regulation and environmental response of flagella in Vibrio journal January 2013
Mechanisms and regulation of surface interactions and biofilm formation in Agrobacterium journal May 2014
Implications of Heat Treatment and Systemic Delivery of Foliar-Applied Oxytetracycline on Citrus Physiological Management and Therapy Delivery journal January 2019

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