Pseudomonas syringae addresses distinct environmental challenges during plant infection through the coordinated deployment of polysaccharides

被引:10
作者
Krishna, Pilla Sankara [1 ]
Woodcock, Stuart Daniel [1 ]
Pfeilmeier, Sebastian [1 ,2 ]
Bornemann, Stephen [2 ,3 ]
Zipfel, Cyril [2 ]
Malone, Jacob George [1 ,4 ]
机构
[1] Norwich Res Pk, Dept Mol Microbiol, John Innes Ctr, Norwich NR4 7UH, Norfolk, England
[2] Univ East Anglia, Sainsbury Lab, Norwich Res Pk, Norwich NR4 7UH, Norfolk, England
[3] Norwich Res Pk, Dept Biol Chem, John Innes Ctr, Norwich NR4 7UH, Norfolk, England
[4] Univ East Anglia, Norwich Res Pk, Norwich NR4 7TJ, Norfolk, England
基金
英国生物技术与生命科学研究理事会; 英国科研创新办公室;
关键词
Biofilm; cyclic-di-GMP; exopolysaccharides; lipopolysaccharide; plant infection Pseudomonas syringae; surface adhesion; ALGINATE GENE-EXPRESSION; PV. TOMATO DC3000; TRANSCRIPTIONAL RESPONSES; EPIPHYTIC FITNESS; BIOFILM FORMATION; GLOBAL REGULATOR; AERUGINOSA; PATHOGEN; VIRULENCE; CELLULOSE;
D O I
10.1093/jxb/erab550
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Pseudomonas syringaeuses the coordinated deployment of polysaccharides to address environmental challenges during plant colonization. Functional redundancy renders individual polysaccharides dispensable during plant infection, but their combined loss impedes pathogenicity. Prior to infection, phytopathogenic bacteria face a challenging environment on the plant surface, where they are exposed to nutrient starvation and abiotic stresses. Pathways enabling surface adhesion, stress tolerance, and epiphytic survival are important for successful plant pathogenesis. Understanding the roles and regulation of these pathways is therefore crucial to fully understand bacterial plant infections. The phytopathogen Pseudomonas syringae pv. tomato (Pst) encodes multiple polysaccharides that are implicated in biofilm formation, stress survival, and virulence in other microbes. To examine how these polysaccharides impact Pst epiphytic survival and pathogenesis, we analysed mutants in multiple polysaccharide loci to determine their intersecting contributions to epiphytic survival and infection. In parallel, we used qRT-PCR to analyse the regulation of each pathway. Pst polysaccharides are tightly coordinated by multiple environmental signals. Nutrient availability, temperature, and surface association strongly affect the expression of different polysaccharides under the control of the signalling protein genes ladS and cbrB and the second messenger cyclic-di-GMP. Furthermore, functionally redundant, combinatorial phenotypes were observed for several polysaccharides. Exopolysaccharides play a role in mediating leaf adhesion, while alpha-glucan and alginate together confer desiccation tolerance. Our results suggest that polysaccharides play important roles in overcoming environmental challenges to Pst during plant infection.
引用
收藏
页码:2206 / 2221
页数:16
相关论文
共 77 条
[1]   Lack of CbrB in Pseudomonas putida affects not only amino acids metabolism but also different stress responses and biofilm development [J].
Amador, Cristina I. ;
Canosa, Ines ;
Govantes, Fernando ;
Santero, Eduardo .
ENVIRONMENTAL MICROBIOLOGY, 2010, 12 (06) :1748-1761
[2]   The ecology and biogeography of microorganisms of plant surfaces [J].
Andrews, JH ;
Harris, RF .
ANNUAL REVIEW OF PHYTOPATHOLOGY, 2000, 38 :145-180
[3]   Cellulose production in Pseudomonas syringae pv. syringae: a compromise between epiphytic and pathogenic lifestyles [J].
Arrebola, Eva ;
Carrion, Victor J. ;
Gutierrez-Barranquero, Jose Antonio ;
Perez-Garcia, Alejandro ;
Rodriguez-Palenzuela, Pablo ;
Cazorla, Francisco M. ;
de Vicente, Antonio .
FEMS MICROBIOLOGY ECOLOGY, 2015, 91 (07)
[4]   The CbrB Regulon: Promoter dissection reveals novel insights into the CbrAB expression network in Pseudomonas putida [J].
Barroso, Rock ;
Garcia-Maurino, Sofia M. ;
Tomas-Gallardo, Laura ;
Andujar, Eloisa ;
Perez-Alegre, Monica ;
Santero, Eduardo ;
Canosa, Ines .
PLOS ONE, 2018, 13 (12)
[5]   Effect of a waaL mutation on lipopolysaccharide composition, oxidative stress survival, and virulence in Erwinia amylovora [J].
Berry, Matthew C. ;
McGhee, Gayle C. ;
Zhao, Youfu ;
Sundin, George W. .
FEMS MICROBIOLOGY LETTERS, 2009, 291 (01) :80-87
[6]   The Extracellular Matrix Component Psl Provides Fast-Acting Antibiotic Defense in Pseudomonas aeruginosa Biofilms [J].
Billings, Nicole ;
Millan, Maria Ramirez ;
Caldara, Marina ;
Rusconi, Roberto ;
Tarasova, Yekaterina ;
Stocker, Roman ;
Ribbeck, Katharina .
PLOS PATHOGENS, 2013, 9 (08)
[7]   Th GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs [J].
Brencic, Anja ;
McFarland, Kirsty A. ;
McManus, Heather R. ;
Castang, Sandra ;
Mogno, Ilaria ;
Dove, Simon L. ;
Lory, Stephen .
MOLECULAR MICROBIOLOGY, 2009, 73 (03) :434-445
[8]   The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000 [J].
Buell, CR ;
Joardar, V ;
Lindeberg, M ;
Selengut, J ;
Paulsen, IT ;
Gwinn, ML ;
Dodson, RJ ;
Deboy, RT ;
Durkin, AS ;
Kolonay, JF ;
Madupu, R ;
Daugherty, S ;
Brinkac, L ;
Beanan, MJ ;
Haft, DH ;
Nelson, WC ;
Davidsen, T ;
Zafar, N ;
Zhou, LW ;
Liu, J ;
Yuan, QP ;
Khouri, H ;
Fedorova, N ;
Tran, B ;
Russell, D ;
Berry, K ;
Utterback, T ;
Van Aken, SE ;
Feldblyum, TV ;
D'Ascenzo, M ;
Deng, WL ;
Ramos, AR ;
Alfano, JR ;
Cartinhour, S ;
Chatterjee, AK ;
Delaney, TP ;
Lazarowitz, SG ;
Martin, GB ;
Schneider, DJ ;
Tang, XY ;
Bender, CL ;
White, O ;
Fraser, CM ;
Collmer, A .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (18) :10181-10186
[9]   Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production [J].
Byrd, Matthew S. ;
Sadovskaya, Irina ;
Vinogradov, Evgueny ;
Lu, Haiping ;
Sprinkle, April B. ;
Richardson, Stephen H. ;
Ma, Luyan ;
Ralston, Brad ;
Parsek, Matthew R. ;
Anderson, Erin M. ;
Lam, Joseph S. ;
Wozniak, Daniel J. .
MOLECULAR MICROBIOLOGY, 2009, 73 (04) :622-638
[10]   Small RNAs and their role in biofilm formation [J].
Chambers, Jacob R. ;
Sauer, Karin .
TRENDS IN MICROBIOLOGY, 2013, 21 (01) :39-49