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

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

doi:10.1094/MPMI-09-21-0230-R

Molecular Plant-Microbe Interactions (Mar 2022)

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

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

Affiliations

Mukesh Jain: Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.
Lulu Cai: Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.
Ian Black: Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, U.S.A.
Parastoo Azadi: Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, U.S.A.
Russell W. Carlson: Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, U.S.A.
Kathryn M. Jones: Department of Biological Science, Florida State University, Tallahassee, FL 32306, U.S.A.
Dean W. Gabriel: Plant Pathology Department, University of Florida, Gainesville, FL 32611, U.S.A.

DOI: https://doi.org/10.1094/MPMI-09-21-0230-R
Journal volume & issue: Vol. 35, no. 3
pp. 257 – 273

Abstract

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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.[Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Published in Molecular Plant-Microbe Interactions

ISSN: 0894-0282 (Print); 1943-7706 (Online)
Publisher: The American Phytopathological Society
Country of publisher: United States
LCC subjects: Science: Microbiology; Science: Botany
Website: https://apsjournals.apsnet.org/journal/mpmi

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