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Defense and virulence defense and evasion mechanisms in the interaction of Pseudomonas syringae with its host plant

Specialized Group:

Javier Ruiz Albert and Carmen R. Beuzón López

Department of Cell Biology, Genetics and Physiology, Institute of Subtropical and Mediterranean Horticulture "La Mayora" - University of Malaga - CSIC (IHSM - UMA - CSIC)

javieruizal@uma.es, cbl@uma.es

Group photo. From left to right, Javier Ruiz-Albert, Diego López-Márquez, Carmen R. Beuzón López, Javier Rueda Blanco, Nieves López Pagán and Ángel del Espino Pérez

 

Group history

The group began its journey in the Genetics Area of ​​the University of Malaga (UMA) in 2003, led by Carmen R. Beuzón and Javier Ruiz Albert, trained at the University of Seville (US), and coming from Imperial College London after a postdoctoral stay in a leading group in the molecular interaction between Salmonella enterica and his guest. Focused on the contribution to virulence of the Type III Secretion System (T3SS), its regulation, and its associated effectors, this work generated numerous publications, some of them references in the field.

The transition to the UMA, determined a change to an analogous theme focused on the molecular interaction of the phytopathogenic bacteria Pseudomonas syringae with its plant hosts, adapting to the new environment, but taking advantage of the experience of previous stages. The group develops research at the molecular level, combining model plant-bacteria pathosystems (Arabidopsis) with pathosystems of agronomic relevance (tomato; bean). The group is part of the founding nucleus of the Institute of Subtropical and Mediterranean Horticulture (IHSM‑UMA‑CSIC). We have obtained uninterrupted funding since 2003 (6 consecutive projects from the National Plan, three excellence projects and one ERDF from the Junta de Andalucía, and a contract with the Fundación Genoma España).

We enjoy numerous collaborations that have given rise to publications with researchers from various national centers such as the IHSM-UMA-CSIC itself, IBMCP-CSIC, EEZ-CSIC, or the US; and numerous international centers such as INRA-CNRS and LRSV-Université de Toulouse, France; FORTH, Greece; CNR, Italy; SIBS, China; Imperial College London, CRIB-UWE, and WISB-University of Warwick; UK; o CIBIO-InBIO-Universidade do Porto, Portugal. These collaborations are extended through our participation in national (RED‑FLAG) and international (HUPLANT-COST Action 16110 and SUSTAIN-COST Action FA1208) networks.

The group constitutes an excellent environment for the training of research staff, helping to start the research career of many students through TFGs and experimental TFMs (>30 defended and several in progress), and Doctoral Theses (8 defended, 3 with an extraordinary doctorate award, and four in progress), including numerous external research stays and with a considerable scientific production per doctoral student. All the graduated doctors are still active in basic or applied research, some with remarkable success.

 

Lines of investigation

Our research focuses on the interaction between pathogenic bacteria P. syringae and the plant, addressing the relevant molecular processes by both the pathogen and the host. We maintain an open and interdisciplinary experimental approach that evolves according to the needs of the projects developed, which allows us to address new questions that open up the field of research. Pathogen-host co-evolution has given rise to bacterial invasion and colonization strategies, with systems dedicated to the introduction of virulence proteins (T3SS) to evade and suppress the corresponding plant defense mechanisms. Our work has included the functional characterization of effectors and their relationship with plant defenses, as well as the regulation of the expression of the virulence system. Among other milestones, we have determined the contribution to virulence of the T3Es repertoire of P. syringae 1448a, one of the main model lineages (1, 2), improving mutant generation techniques and developing genetic analysis techniques in planta (competitive index, CIs) (3 and references included). We have been the first to describe the suppression capacity of all levels of plant defense (PTI, ETI, and SAR) by an effector, HopZ1, analyzing the signal transduction pathways involved in its recognition in resistant plants (4), and characterized in its natural pathosystem the defense suppression capacity of the effector of the same HopZ3 family (5).

We have described mechanisms of positive and negative regulation of the expression of T3SS genes in Pph1448a (6, Ferrándiz MJ, Martín-Galiano AJ, Arnanz C, Camacho-Soguero I, Tirado-Vélez JM, de la Campa AG.), and collaborated in establishing a link between regulation of expression and secretion (8). We have described for the first time in a phytopathogen phenotypic heterogeneity in the expression of T3SS (Assay validation) and the flagellum, giving rise to bacterial lineages that differ in the expression of these key aspects of virulence. P. syringae. We have also described the dynamics, clonality and interactions of mixed populations in planta (Granting of 5 FEMS scholarships to young SEM researchers).

Additional lines in collaboration with other groups, around the characterization of the interference between geminivirus and sumoylation in the plant, in collaboration with Eduardo R. Bejarano (IHSM-UMA-CSIC) and Herlander Azevedo (Universidade do Porto) has led to five articles, while the development of genomic tools in olive trees and their application to fruit and oil quality, and traits of agronomic interest, within the OLEAGEN (Genome Spain) consortium, has led to another five articles.

 

Future perspectives

In our current project of the National Plan (RTI2018-095069-B-I00) we are analyzing the methylome of P. syringae under laboratory and plant conditions and looking for candidate loci to present phenotypic heterogeneity. We have identified and are characterizing the DNA methylases potentially associated with such regulation. We are expanding our characterization of the role of phenotypic heterogeneity in the adaptation of P. syringae to the plant, exploring potential biotechnological applications.

Within the same project, and in collaboration with the group of Josep Casadesús (US), we analyzed the role of phenotypic heterogeneity during the colonization of the plant by Salmonella, associated with more than 25% of epidemic outbreaks of salmonellosis (CDC-USA), due to internal contamination of fresh fruit and vegetables intended for consumption. This line takes advantage of the experience in Salmonella of the principal investigators prior to the formation of the group, combined with their experience in pathogenesis in plants accumulated since then.

Finally, in the context of an FEDER project and our collaboration with Eduardo R. Bejarano's group (IHSM-UMA-CSIC), we are characterizing a regulatory mechanism in the plant that controls the expression of TIR-NBS-LRR genes in the absence of pathogens, limiting their impact on fitness of the plant, allowing its activation in two waves in the presence of pathogens. This inducible defense mechanism, not linked to a single avirulence gene, has great potential for the development of efficient and robust resistance strategies.

 

Representative bibliography

  1. View Article PubMed PubMed Central Google Scholar Zumaquero A, Macho AP, Ruffian JS, Beuzon CR (2010). Pseudomonas syringae pv. phaseolicola 1448a in interaction with the plant. J Bacteriol. 192(17):4474-88.
  2. View Article PubMed PubMed Central Google Scholar Macho AP, Zumaquero A, Gonzalez-Plaza JJ, Ortiz-Martin I, Rufian JS, Beuzon CR (2012). Pseudomonas syringae pv. phaseolicola. PLoS ONE 7: e35871.
  3. Macho AP, Rufián JS, Ruiz‑Albert J, Beuzón CR (2016) Competitive Index: Mixed Infection-Based Virulence Assays for Genetic Analysis in Pseudomonas syringae-Plant Interactions. In: Botella J., Botella M. (eds) Plant Signal Transduction. Methods in Molecular Biology, 1363: 209-17, Humana Press, New York, NY
  4. Macho AP, Guevara CM, Tornero P, Ruiz-Albert J, Beuzón CR (2010) The Pseudomonas syringae effector proteín HopZ1a suppresses effector-triggered immunity. New Phytologist. 187:1018-1033.
  5. Rufián JS, Lucía A, Rueda-Blanco J, Zumaquero A, Guevara CM, Ortiz-Martín I, Ruiz-Aldea G, Macho AP, Beuzón CR, Ruiz-Albert J. (2018) Suppression of HopZ Effector-triggered Plant Immunity in a natural pathosystem. Front Plan Sci 14:977.
  6. Ortiz-Martín I, Thwaites R, Mansfield JW, Beuzón CR (2010) Negative Regulation of the Hrp Type III Secretion System in Pseudomonas syringae pv. phaseolicola. Mol Plant–Microbe Interact. 23:682-701.
  7. Ortiz-Martín I, Thwaites R, Macho AP, Mansfield JW, Beuzón CR (2010) Positive Regulation of the Hrp Type III Secretion System in Pseudomonas syringae pv. phaseolicola. Molecular Plant –Microbe Interactions. 23:665-681.
  8. Charova SN, Gazi AD, Mylonas E, Pozidis C, Sabarit B, Anagnostou D, Psatha K, Aivaliotis M, Beuzon CR, Panopoulos NJ, Kokkinidis M.(2018) Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion. mBio 31:9 pii: e01096-18.
  9. Rufián JS, Sánchez-Romero M-A, López-Márquez D, Macho AP, Mansfield JW, Arnold DL, Ruiz-Albert J, Casadesús J, Beuzón CR, (2016) Pseudomonas syringae differentiates into phenotypically distinct subpopulations during colonization of a plant host. Environ microbiol.
  10. Rufián JS, Macho AP, Corry DS, Mansfield JW, Ruiz-Albert J, Arnold DL, Beuzón CR, (2018) Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non-pathogenic Pseudomonas syringae strains. Mol Plant Pathol.
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