‘Candidatus Liberibacter asiaticus’-Encoded BCP Peroxiredoxin Suppresses Lipopolysaccharide-Mediated Defense Signaling and Nitrosative Stress In Planta

Jain, Mukesh; Cai, Lulu; Black, Ian; Azadi, Parastoo; Carlson, Russell W.; Jones, Kathryn M.; Gabriel, Dean W.

doi:10.1094/mpmi-09-21-0230-r

‘Candidatus Liberibacter asiaticus’-Encoded BCP Peroxiredoxin Suppresses Lipopolysaccharide-Mediated Defense Signaling and Nitrosative Stress In Planta

Journal Article · Thu Mar 10 04:00:00 EST 2022 · Molecular Plant-Microbe Interactions

DOI:https://doi.org/10.1094/mpmi-09-21-0230-r· OSTI ID:1963234

Jain, Mukesh ^[1]; Cai, Lulu ^[2]; Black, Ian ^[3]; Azadi, Parastoo ^[3]; Carlson, Russell W. ^[3]; ^[4]; ^[2]

Univ. of Florida, Gainesville, FL (United States); University of Florida
Univ. of Florida, Gainesville, FL (United States)
Univ. of Georgia, Athens, GA (United States)
Florida State Univ., Tallahassee, FL (United States)

The lipopolysaccharides (LPS) of gram-negative bacteria trigger a nitrosative and oxidative burst in both animals and plants during pathogen invasion. Liberibacter crescens strain BT-1 is a surrogate for functional genomic studies of the uncultured pathogenic ‘Candidatus Liberibacter’ spp. that are associated with severe diseases such as citrus greening and potato zebra chip. Structural determination of L. crescens LPS revealed the presence of a very long chain fatty acid modification. L. crescens LPS pretreatment suppressed growth of Xanthomonas perforans on nonhost tobacco (Nicotiana benthamiana) and X. citri subsp. citri on host orange (Citrus sinensis), confirming bioactivity of L. crescens LPS in activation of systemic acquired resistance (SAR). L. crescens LPS elicited a rapid burst of nitric oxide (NO) in suspension cultured tobacco cells. Pharmacological inhibitor assays confirmed that arginine-utilizing NO synthase (NOS) activity was the primary source of NO generation elicited by L. crescens LPS. LPS treatment also resulted in biological markers of NO-mediated SAR activation, including an increase in the glutathione pool, callose deposition, and activation of the salicylic acid and azelaic acid (AzA) signaling networks. Transient expression of ‘Ca. L. asiaticus’ bacterioferritin comigratory protein (BCP) peroxiredoxin in tobacco compromised AzA signaling, a prerequisite for LPS-triggered SAR. Western blot analyses revealed that ‘Ca. L. asiaticus’ BCP peroxiredoxin prevented peroxynitrite-mediated tyrosine nitration in tobacco. ‘Ca. L. asiaticus’ BCP peroxiredoxin (i) attenuates NO-mediated SAR signaling and (ii) scavenges peroxynitrite radicals, which would facilitate repetitive cycles of ‘Ca. L. asiaticus’ acquisition and transmission by fecund psyllids throughout the limited flush period in citrus.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Institute of Food and Agriculture Specialty Crops Research Initiative (NIFA-SCRI)

Grant/Contract Number:: SC0015662

OSTI ID:: 1963234

Journal Information:: Molecular Plant-Microbe Interactions, Journal Name: Molecular Plant-Microbe Interactions Journal Issue: 3 Vol. 35; ISSN 0894-0282

Publisher:: APS Press - International Society for Molecular Plant-Microbe InteractionsCopyright Statement

Country of Publication:: United States

Language:: English

References (82)

The Acylation and Phosphorylation Pattern of Lipid A fromXanthomonas Campestris Strongly Influence its Ability to Trigger the Innate Immune Response in Arabidopsis Silipo, Alba; Sturiale, Luisa; Garozzo, Domenico ChemBioChem, Vol. 9, Issue 6 https://doi.org/10.1002/cbic.200700693	journal	April 2008
Do nitric oxide donors mimic endogenous NO-related response in plants? Floryszak-Wieczorek, J.; Milczarek, G.; Arasimowicz, M. Planta, Vol. 224, Issue 6 https://doi.org/10.1007/s00425-006-0321-1	journal	June 2006
Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection Dong, Xiaoyun; Hong, Zonglie; Chatterjee, Jayanta Planta, Vol. 229, Issue 1 https://doi.org/10.1007/s00425-008-0812-3	journal	September 2008
A survey of ‘Candidatus Liberibacter solanacearum’ in historical seed from collections of carrot and related Apiaceae species Monger, Wendy A.; Jeffries, Colin J. European Journal of Plant Pathology, Vol. 150, Issue 3 https://doi.org/10.1007/s10658-017-1322-6	journal	September 2017
Structure, biosynthesis and function of unusual lipids A from nodule-inducing and N 2 -fixing bacteria Choma, Adam; Komaniecka, Iwona; Zebracki, Kamil Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1862, Issue 2 https://doi.org/10.1016/j.bbalip.2016.11.004	journal	February 2017
S-nitrosylation influences the structure and DNA binding activity of AtMYB30 transcription factor from Arabidopsis thaliana Tavares, Carolina Pereira; Vernal, Javier; Delena, Ricardo Alexandre Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1844, Issue 4 https://doi.org/10.1016/j.bbapap.2014.02.015	journal	April 2014
Untargeted metabolomics analysis reveals dynamic changes in azelaic acid- and salicylic acid derivatives in LPS-treated Nicotiana tabacum cells Mhlongo, M. I.; Tugizimana, F.; Piater, L. A. Biochemical and Biophysical Research Communications, Vol. 482, Issue 4 https://doi.org/10.1016/j.bbrc.2016.12.063	journal	January 2017
Host-free biofilm culture of “Candidatus Liberibacter asiaticus,” the bacterium associated with Huanglongbing Ha, Phuc T.; He, Ruifeng; Killiny, Nabil Biofilm, Vol. 1 https://doi.org/10.1016/j.bioflm.2019.100005	journal	December 2019
A Feedback Regulatory Loop between G3P and Lipid Transfer Proteins DIR1 and AZI1 Mediates Azelaic-Acid-Induced Systemic Immunity Yu, Keshun; Soares, Juliana Moreira; Mandal, Mihir Kumar Cell Reports, Vol. 3, Issue 4 https://doi.org/10.1016/j.celrep.2013.03.030	journal	April 2013
Mono- and Digalactosyldiacylglycerol Lipids Function Nonredundantly to Regulate Systemic Acquired Resistance in Plants Gao, Qing-ming; Yu, Keshun; Xia, Ye Cell Reports, Vol. 9, Issue 5 https://doi.org/10.1016/j.celrep.2014.10.069	journal	December 2014
Growth of ‘Candidatus Liberibacter asiaticus’ in a host-free microbial culture is associated with microbial community composition Molki, Banafsheh; Call, Douglas R.; Ha, Phuc T. Enzyme and Microbial Technology, Vol. 142 https://doi.org/10.1016/j.enzmictec.2020.109691	journal	December 2020
Signaling and stress: The redox landscape in NOS2 biology Thomas, Douglas D.; Heinecke, Julie L.; Ridnour, Lisa A. Free Radical Biology and Medicine, Vol. 87 https://doi.org/10.1016/j.freeradbiomed.2015.06.002	journal	October 2015
Toll-like Receptors and Their Crosstalk with Other Innate Receptors in Infection and Immunity Kawai, Taro; Akira, Shizuo Immunity, Vol. 34, Issue 5 https://doi.org/10.1016/j.immuni.2011.05.006	journal	May 2011
‘Candidatus Liberibacter asiaticus’ peroxiredoxin (LasBCP) suppresses oxylipin-mediated defense signaling in citrus Jain, Mukesh; Munoz-Bodnar, Alejandra; Gabriel, Dean W. Journal of Plant Physiology, Vol. 236 https://doi.org/10.1016/j.jplph.2019.03.001	journal	May 2019
Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing Li, Wenbin; Hartung, John S.; Levy, Laurene Journal of Microbiological Methods, Vol. 66, Issue 1 https://doi.org/10.1016/j.mimet.2005.10.018	journal	July 2006
Sensing of molecular patterns through cell surface immune receptors Ranf, Stefanie Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.011	journal	August 2017
Gene expression in Citrus sinensis (L.) Osbeck following infection with the bacterial pathogen Candidatus Liberibacter asiaticus causing Huanglongbing in Florida Albrecht, Ute; Bowman, Kim D. Plant Science, Vol. 175, Issue 3 https://doi.org/10.1016/j.plantsci.2008.05.001	journal	September 2008
Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses Wimalasekera, Rinukshi; Tebartz, Felix; Scherer, Günther F. E. Plant Science, Vol. 181, Issue 5 https://doi.org/10.1016/j.plantsci.2011.04.002	journal	November 2011
Metabolite signature of the phloem sap of fourteen citrus varieties with different degrees of tolerance to Candidatus Liberibacter asiaticus Killiny, Nabil Physiological and Molecular Plant Pathology, Vol. 97 https://doi.org/10.1016/j.pmpp.2016.11.004	journal	January 2017
Citrus phytohormonal response to Candidatus Liberibacter asiaticus and its vector Diaphorina citri Nehela, Yasser; Hijaz, Faraj; Elzaawely, Abdelnaser A. Physiological and Molecular Plant Pathology, Vol. 102 https://doi.org/10.1016/j.pmpp.2017.11.004	journal	April 2018
Plant Immunity: Thinking Outside and Inside the Box van der Burgh, Aranka M.; Joosten, Matthieu H. A. J. Trends in Plant Science, Vol. 24, Issue 7 https://doi.org/10.1016/j.tplants.2019.04.009	journal	July 2019
Kinetic and Thermodynamic Features Reveal That Escherichia coli BCP Is an Unusually Versatile Peroxiredoxin Reeves, Stacy A.; Parsonage, Derek; Nelson, Kimberly J. Biochemistry, Vol. 50, Issue 41 https://doi.org/10.1021/bi200935d	journal	October 2011
S-nitrosylation of NADPH oxidase regulates cell death in plant immunity Yun, Byung-Wook; Feechan, Angela; Yin, Minghui Nature, Vol. 478, Issue 7368 https://doi.org/10.1038/nature10427	journal	October 2011
A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana Ranf, Stefanie; Gisch, Nicolas; Schäffer, Milena Nature Immunology, Vol. 16, Issue 4 https://doi.org/10.1038/ni.3124	journal	March 2015
An effector from the Huanglongbing-associated pathogen targets citrus proteases Clark, Kelley; Franco, Jessica Yvette; Schwizer, Simon Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04140-9	journal	April 2018
Arabidopsis LBP/BPI related-1 and -2 bind to LPS directly and regulate PR1 expression Iizasa, Sayaka; Iizasa, Ei’ichi; Matsuzaki, Sawako Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep27527	journal	June 2016
Suppression of an elicitor‐induced oxidative burst reaction in Medicago sativa cell cultures by Sinorhizobium meliloti lipopolysaccharides Albus, Ulrike; Baier, Ruth; Holst, Otto New Phytologist, Vol. 151, Issue 3 https://doi.org/10.1046/j.0028-646x.2001.00214.x	journal	September 2001
The role of lipopolysaccharides in induction of plant defence responses Erbs, Gitte; Newman, Mari-Anne Molecular Plant Pathology, Vol. 4, Issue 5 https://doi.org/10.1046/j.1364-3703.2003.00179.x	journal	September 2003
Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids Ferguson, Gail P.; Datta, Anup; Baumgartner, John Proceedings of the National Academy of Sciences, Vol. 101, Issue 14 https://doi.org/10.1073/pnas.0307137101	journal	March 2004
Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity Forouhar, F.; Yang, Y.; Kumar, D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 5 https://doi.org/10.1073/pnas.0409227102	journal	January 2005
An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane Malinverni, J. C.; Silhavy, T. J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 19 https://doi.org/10.1073/pnas.0903229106	journal	April 2009
Modeling huanglongbing transmission within a citrus tree Chiyaka, Christinah; Singer, Burton H.; Halbert, Susan E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 30 https://doi.org/10.1073/pnas.1208326109	journal	July 2012
Asymptomatic spread of huanglongbing and implications for disease control Lee, Jo Ann; Halbert, Susan E.; Dawson, William O. Proceedings of the National Academy of Sciences, Vol. 112, Issue 24 https://doi.org/10.1073/pnas.1508253112	journal	June 2015
Structural and Biochemical Characterization of Peroxiredoxin Qβ from Xylella fastidiosa Horta, Bruno Brasil; de Oliveira, Marcos Antonio; Discola, Karen Fulan Journal of Biological Chemistry, Vol. 285, Issue 21 https://doi.org/10.1074/jbc.M109.094839	journal	May 2010
Multilevel Regulation of 2-Cys Peroxiredoxin Reaction Cycle by S-Nitrosylation Engelman, Rotem; Weisman-Shomer, Pnina; Ziv, Tamar Journal of Biological Chemistry, Vol. 288, Issue 16 https://doi.org/10.1074/jbc.M112.433755	journal	April 2013
Sinorhizobium meliloti acpXL Mutant Lacks the C28 Hydroxylated Fatty Acid Moiety of Lipid A and Does Not Express a Slow Migrating Form of Lipopolysaccharide Sharypova, Larissa A.; Niehaus, Karsten; Scheidle, Heiko Journal of Biological Chemistry, Vol. 278, Issue 15 https://doi.org/10.1074/jbc.M209389200	journal	April 2003
Metacaspase Activity of Arabidopsis thaliana Is Regulated by S -Nitrosylation of a Critical Cysteine Residue Belenghi, Beatrice; Romero-Puertas, Maria C.; Vercammen, Dominique Journal of Biological Chemistry, Vol. 282, Issue 2 https://doi.org/10.1074/jbc.M608931200	journal	November 2006
Nitric oxide in plants: an assessment of the current state of knowledge Mur, L. A. J.; Mandon, J.; Persijn, S. AoB Plants, Vol. 5, Issue 0 https://doi.org/10.1093/aobpla/pls052	journal	December 2012
In vivo protein tyrosine nitration in Arabidopsis thaliana Lozano-Juste, Jorge; Colom-Moreno, Rosa; León, José Journal of Experimental Botany, Vol. 62, Issue 10 https://doi.org/10.1093/jxb/err042	journal	March 2011
Nitric oxide production in plants: an update Astier, Jeremy; Gross, Inonge; Durner, Jörg Journal of Experimental Botany, Vol. 69, Issue 14 https://doi.org/10.1093/jxb/erx420	journal	December 2017
A physiological perspective on targets of nitration in NO-based signaling networks in plants Arasimowicz-Jelonek, Magdalena; Floryszak-Wieczorek, Jolanta Journal of Experimental Botany, Vol. 70, Issue 17 https://doi.org/10.1093/jxb/erz300	journal	July 2019
A Secreted ‘Candidatus Liberibacter asiaticus’ Peroxiredoxin Simultaneously Suppresses Both Localized and Systemic Innate Immune Responses In Planta Jain, Mukesh; Munoz-Bodnar, Alejandra; Zhang, Shujian Molecular Plant-Microbe Interactions®, Vol. 31, Issue 12 https://doi.org/10.1094/MPMI-03-18-0068-R	journal	December 2018
Sec-Delivered Effector 1 (SDE1) of ‘Candidatus Liberibacter asiaticus’ Promotes Citrus Huanglongbing Clark, Kelley J.; Pang, Zhiqian; Trinh, Jessica Molecular Plant-Microbe Interactions®, Vol. 33, Issue 12 https://doi.org/10.1094/MPMI-05-20-0123-R	journal	December 2020
Prophage-Encoded Peroxidase in ‘Candidatus Liberibacter asiaticus’ Is a Secreted Effector That Suppresses Plant Defenses Jain, Mukesh; Fleites, Laura A.; Gabriel, Dean W. Molecular Plant-Microbe Interactions®, Vol. 28, Issue 12 https://doi.org/10.1094/MPMI-07-15-0145-R	journal	December 2015
The Complete Genome Sequence of ‘ Candidatus Liberibacter americanus’, Associated with Citrus Huanglongbing Wulff, Nelson A.; Zhang, Shujian; Setubal, João C. Molecular Plant-Microbe Interactions, Vol. 27, Issue 2 https://doi.org/10.1094/MPMI-09-13-0292-R	journal	February 2014
‘Candidatus Liberibacter asiaticus’ and Its Vector, Diaphorina citri, Augment the Tricarboxylic Acid Cycle of Their Host via the γ-Aminobutyric Acid Shunt and Polyamines Pathway Nehela, Yasser; Killiny, Nabil Molecular Plant-Microbe Interactions®, Vol. 32, Issue 4 https://doi.org/10.1094/MPMI-09-18-0238-R	journal	April 2019
‘ Candidatus Liberibacter asiaticus’ Encodes a Functional Salicylic Acid (SA) Hydroxylase That Degrades SA to Suppress Plant Defenses Li, Jinyun; Pang, Zhiqian; Trivedi, Pankaj Molecular Plant-Microbe Interactions, Vol. 30, Issue 8 https://doi.org/10.1094/MPMI-12-16-0257-R	journal	August 2017
Progress and Obstacles in Culturing ‘Candidatus Liberibacter asiaticus’, the Bacterium Associated with Huanglongbing Merfa, Marcus V.; Pérez-López, Edel; Naranjo, Eber Phytopathology®, Vol. 109, Issue 7 https://doi.org/10.1094/PHYTO-02-19-0051-RVW	journal	July 2019
Liberibacter crescens Is a Cultured Surrogate for Functional Genomics of Uncultured Pathogenic ‘Candidatus Liberibacter’ spp. and Is Naturally Competent for Transformation Jain, M.; Cai, L.; Fleites, L. A. Phytopathology®, Vol. 109, Issue 10 https://doi.org/10.1094/PHYTO-04-19-0129-R	journal	October 2019
Response of Sweet Orange ( Citrus sinensis ) to ‘ Candidatus Liberibacter asiaticus’ Infection: Microscopy and Microarray Analyses Kim, Jeong-Soon; Sagaram, Uma Shankar; Burns, Jacqueline K. Phytopathology, Vol. 99, Issue 1 https://doi.org/10.1094/PHYTO-99-1-0050	journal	January 2009
Chloroplasts as a Nitric Oxide Cellular Source. Effect of Reactive Nitrogen Species on Chloroplastic Lipids and Proteins Jasid, Sebastián; Simontacchi, Marcela; Bartoli, Carlos G. Plant Physiology, Vol. 142, Issue 3 https://doi.org/10.1104/pp.106.086918	journal	September 2006
Lipid Profiling of the Arabidopsis Hypersensitive Response Reveals Specific Lipid Peroxidation and Fragmentation Processes: Biogenesis of Pimelic and Azelaic Acid Zoeller, Maria; Stingl, Nadja; Krischke, Markus Plant Physiology, Vol. 160, Issue 1 https://doi.org/10.1104/pp.112.202846	journal	July 2012
Lipopolysaccharides Trigger Two Successive Bursts of Reactive Oxygen Species at Distinct Cellular Locations Shang-Guan, Keke; Wang, Min; Htwe, Nang Myint Phyu Sin Plant Physiology, Vol. 176, Issue 3 https://doi.org/10.1104/pp.17.01637	journal	February 2018
Citrus CsACD2 Is a Target of Candidatus Liberibacter Asiaticus in Huanglongbing Disease Pang, Zhiqian; Zhang, Li; Coaker, Gitta Plant Physiology, Vol. 184, Issue 2 https://doi.org/10.1104/pp.20.00348	journal	August 2020
Redox Regulation of the NPR1-TGA1 System of Arabidopsis thaliana by Nitric Oxide Lindermayr, Christian; Sell, Simone; Müller, Bernd The Plant Cell, Vol. 22, Issue 8 https://doi.org/10.1105/tpc.109.066464	journal	August 2010
Characterization of a Nitric Oxide Synthase from the Plant Kingdom: NO Generation from the Green Alga Ostreococcus tauri Is Light Irradiance and Growth Phase Dependent Foresi, Noelia; Correa-Aragunde, Natalia; Parisi, Gustavo The Plant Cell, Vol. 22, Issue 11 https://doi.org/10.1105/tpc.109.073510	journal	November 2010
Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity Návarová, Hana; Bernsdorff, Friederike; Döring, Anne-Christin The Plant Cell, Vol. 24, Issue 12 https://doi.org/10.1105/tpc.112.103564	journal	December 2012
Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis Ferguson, Gail P.; Datta, Anup; Carlson, Russ W. Molecular Microbiology, Vol. 56, Issue 1 https://doi.org/10.1111/j.1365-2958.2005.04536.x	journal	February 2005
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
Genome‐wide analyses of Liberibacter species provides insights into evolution, phylogenetic relationships, and virulence factors Thapa, Shree P.; De Francesco, Agustina; Trinh, Jessica Molecular Plant Pathology, Vol. 21, Issue 5 https://doi.org/10.1111/mpp.12925	journal	February 2020
Production, amplification and systemic propagation of redox messengers in plants? The phloem can do it all! Gaupels, Frank; Durner, Jörg; Kogel, Karl‐Heinz New Phytologist, Vol. 214, Issue 2 https://doi.org/10.1111/nph.14399	journal	January 2017
TGACG-BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 ( SARD1 ) and CALMODULIN-BINDING PROTEIN 60g ( CBP60g ) Sun, Tongjun; Busta, Lucas; Zhang, Qian New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14780	journal	September 2017
OsCERK1 plays a crucial role in the lipopolysaccharide-induced immune response of rice Desaki, Yoshitake; Kouzai, Yusuke; Ninomiya, Yusuke New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14941	journal	November 2017
Systemic propagation of immunity in plants Vlot, A. Corina; Sales, Jennifer H.; Lenk, Miriam New Phytologist, Vol. 229, Issue 3 https://doi.org/10.1111/nph.16953	journal	October 2020
Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress Tanou, Georgia; Ziogas, Vasileios; Belghazi, Maya Plant, Cell & Environment, Vol. 37, Issue 4 https://doi.org/10.1111/pce.12204	journal	October 2013
Pipecolic acid confers systemic immunity by regulating free radicals Wang, Caixia; Liu, Ruiying; Lim, Gah-Hyun Science Advances, Vol. 4, Issue 5 https://doi.org/10.1126/sciadv.aar4509	journal	May 2018
Plant Immunity Requires Conformational Charges of NPR1 via S-Nitrosylation and Thioredoxins Tada, Y.; Spoel, S. H.; Pajerowska-Mukhtar, K. Science, Vol. 321, Issue 5891 https://doi.org/10.1126/science.1156970	journal	August 2008
Priming in Systemic Plant Immunity Jung, Ho Won; Tschaplinski, Timothy J.; Wang, Lin Science, Vol. 324, Issue 5923 https://doi.org/10.1126/science.1170025	journal	April 2009
Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants Castillo, Mari-Cruz; Lozano-Juste, Jorge; González-Guzmán, Miguel Science Signaling, Vol. 8, Issue 392 https://doi.org/10.1126/scisignal.aaa7981	journal	September 2015
Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom Jeandroz, Sylvain; Wipf, Daniel; Stuehr, Dennis J. Science Signaling, Vol. 9, Issue 417 https://doi.org/10.1126/scisignal.aad4403	journal	March 2016
Pathogen Recognition and Inflammatory Signaling in Innate Immune Defenses Mogensen, T. H. Clinical Microbiology Reviews, Vol. 22, Issue 2 https://doi.org/10.1128/CMR.00046-08	journal	April 2009
Current Epidemiological Understanding of Citrus Huanglongbing Gottwald, Tim R. Annual Review of Phytopathology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev-phyto-073009-114418	journal	July 2010
The Induction and Modulation of Plant Defense Responses by Bacterial Lipopolysaccharides Dow, Max; Newman, Mari-Anne; von Roepenack, Edda Annual Review of Phytopathology, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.phyto.38.1.241	journal	September 2000
Transcriptome analysis reveals key roles of AtLBR-2 in LPS-induced defense responses in plants Iizasa, Sayaka; Iizasa, Ei’ichi; Watanabe, Keiichi BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4372-4	journal	December 2017
Discovery of new biosynthetic pathways: the lipid A story Raetz, Christian R. H.; Guan, Ziqiang; Ingram, Brian O. Journal of Lipid Research, Vol. 50, Issue Supplement https://doi.org/10.1194/jlr.R800060-JLR200	journal	October 2008
GPS-SNO: Computational Prediction of Protein S-Nitrosylation Sites with a Modified GPS Algorithm Xue, Yu; Liu, Zexian; Gao, Xinjiao PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011290	journal	June 2010
Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity Schwartz, Allison R.; Potnis, Neha; Timilsina, Sujan Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00535	journal	June 2015
Alterations of Candidatus Liberibacter asiaticus-Associated Microbiota Decrease Survival of Ca. L. asiaticus in in vitro Assays Fujiwara, Kazuki; Iwanami, Toru; Fujikawa, Takashi Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03089	journal	December 2018
A Sec-Dependent Secretory Protein of the Huanglongbing-Associated Pathogen Suppresses Hypersensitive Cell Death in Nicotiana benthamiana Zhang, Chao; Du, Peixiu; Yan, Hailin Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.594669	journal	November 2020
Nitric Oxide-Dependent Posttranslational Modification in Plants: An Update Astier, Jeremy; Lindermayr, Christian International Journal of Molecular Sciences, Vol. 13, Issue 12 https://doi.org/10.3390/ijms131115193	journal	November 2012
Structure of Lipopolysaccharide from Liberibacter crescens Is Low Molecular Weight and Offers Insight into Candidatus Liberibacter Biology Black, Ian M.; Heiss, Christian; Jain, Mukesh International Journal of Molecular Sciences, Vol. 22, Issue 20 https://doi.org/10.3390/ijms222011240	journal	October 2021
Complete genome sequence of Liberibacter crescens BT-1 Leonard, Michael T.; Fagen, Jennie R.; Davis-Richardson, Austin G. Standards in Genomic Sciences, Vol. 7, Issue 2 https://doi.org/10.4056/sigs.3326772	journal	December 2012

Similar Records

Linking metabolic phenotypes to pathogenic traits among “Candidatus Liberibacter asiaticus” and its hosts

Journal Article · Tue Aug 04 00:00:00 EDT 2020 · npj Systems Biology and Applications · OSTI ID:1802443

Structure of Lipopolysaccharide from Liberibacter crescens Is Low Molecular Weight and Offers Insight into Candidatus Liberibacter Biology

Journal Article · Mon Oct 18 00:00:00 EDT 2021 · International Journal of Molecular Sciences (Online) · OSTI ID:1963261

Comparative Genomics of Cultured and Uncultured Strains Suggests Genes Essential for Free-Living Growth of Liberibacter

Journal Article · Tue Jan 07 23:00:00 EST 2014 · PLoS ONE · OSTI ID:1627668

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Bacteria-plant symbiosis
Bacterial pathogenesis
Citrus greening
Effectors
Elicitors
Ethylene
Huanglongbing
Innate immunity
Jasmonic acid
Liberibacter
Lipid A
Lipopolysaccharide
Molecular signaling
Nitric oxide
Plant responses to pathogens
Salicylic acid
Systemic acquired resistance
Zebra chip

‘Candidatus Liberibacter asiaticus’-Encoded BCP Peroxiredoxin Suppresses Lipopolysaccharide-Mediated Defense Signaling and Nitrosative Stress In Planta

Citation Formats

References (82)

Similar Records

Related Subjects