PHYTOPATHOGENIC BACTERIA

Group leader: Emilia López Solanilla - Professor
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Personnel:

 

  

Research interest

Bacterial plant diseases are responsible for considerable economic losses associated with crop production. The list of antimicrobial substances currently available to fight bacterial plant diseases is scarce. In addition, there is an increasing trend of bacterial resistance to existing bactericides. These facts, together with the threat of outbreak of bacterial plant diseases as a consequence of climate change, makes the development of sustainable alternatives to fight bacterial diseases a research priority in the plant protection area.

         

For more than a decade, our group has been involved in the study of the early stages of infection by bacterial plant pathogens. Phytopathogenic bacteria colonize plant surfaces and can multiply epiphytically and saprophytically before entering the plant tissue. When conditions are favorable, bacteria enter through natural openings or wounds and multiply in plant apoplast activating virulence mechanisms and inducing the symptoms associated with the disease. These initial phases, when bacteria adapt to host environment and deal with the entry into the plant apoplast, determine the success of the infection and are therefore prime targets for interfering with disease development.
Chemotaxis and bacterial entry into the host plant

 

 

              

Chemosensory functions and pathogenicity

Chemosensory pathways represent one of the primary bacterial signal transduction systems, are widely distributed among bacteria and exert a key role in signal transduction processes associated with the response to environmental cues. The core of a chemosensory pathway is formed by a complex composed of a chemoreceptor (CR), or methyl-accepting chemotaxis protein (MCP), the CheA histidine kinase, and the CheW adaptor protein.
                     

The minimal signaling unit contains two trimers of homodimeric receptor dimers connected by a CheA dimer and two CheW monomers. In the canonical pathway, signal (chemoeffector) binding to the CR ligand binding domain (LBD) creates a molecular stimulus that modulates CheA autophosphorylation activity, which in turn alters the transphosphorylation activity of the response regulator CheY. In the case of a chemotaxis pathway, phosphorylated CheY (CheY-P) binds to the flagellar motor, controlling the direction of flagellar rotation and ultimately bacterial motility. Although most chemosensory pathways appear to be involved in chemotaxis, other pathways have been found to be associated with type IV pilus-based motility or the control of cyclic diguanosine monophosphate (c-di-GMP) and cyclic adenosine monophosphate (c-AMP) second messenger levels.

 

Our research aims to understand the significance in disease production of the mechanisms underlying the perception and response to plant and environmental signals within two model phytopathogenic bacteria that exhibit distinct pathogenic styles: the hemibiotrophic bacteria Pseudomonas syringae pv. tomato DC3000 (PsPto), which is the causal agent of bacterial speck in tomato, and Dickeya dandantii 3937 (Dd3937), a necrotroph soft-rot enterobacterium which has a broad-host range. Specifically, we are interested in the role of chemosensory functions in the regulation of the entry process and establishment of infection in the host.

 
(Cerna-Vargas et al., 2019)

(Gálvez-Roldán et al., 2023)

  

                                                                                                                                                                                              

Characterization of bacterial chemoreceptors involved in plant interaction

 

We have carried out a comprehensive phylogenomic analysis of the full CR repertoire from a wide collection of microbial genomes. We have identified CR ligand-binding domains (LBDs) with high degree of plant association that are shared across distant taxonomic ranges and are postulated to be strong biomarkers for the plant-associated lifestyle.

 


Schematic view of the bioinformatics pipeline used to identify CRs that are potentially relevant for plant association (Sanchis-López et al., 2021)

 

We work with selected chemoreceptors from our two model bacteria for an in-depth biochemical and functional characterization.

In PsPto, we have described the function of a chemoreceptor (PscA) involved in the perception of L-Asp, D-Asp and L-Glu that mediates the regulation of virulence-related traits through the control of c-di-GMP levels. Results suggest a crosstalk between signal perception and virulence-related mechanisms to elaborate a coordinated response that optimizes PsPto virulence.
 (Cerna-Vargas et al., 2019)

 

 


We have also characterized a GABA and L-Pro CR which function is related with the virulence of PsPto in tomato plants. The perception of these abundant compounds, whose concentrations increase during infection, drives the entry of PsPto into apoplast and regulates the expression of genes involved in GABA catabolism.

 

In Dd3937, our efforts are focused on the study of the perception of nitrate/nitrite and plant cell wall-derived compounds. We have found that the perception of these kind of compounds is relevant for the full virulence of this pathogen, determining not only bacterial entry but also the regulation of virulence traits.

 

We are characterizing selected chemoreceptors in both bacterial models to unveil the specific functions in the interaction with plant host.

Overall, our results point to the potential use of non-metabolizable chemoeffectors as interfering tools to prevent bacterial infection.


(Cerna-Vargas et al., 2019)



"Energy taxis” and bacterial pathogenesis

“Energy taxis” is a process which allows the navigation to niches that support maximum energy levels. We are working on determine how phytobacteria deal with the perception of poor nutritional environments and how bacteria transduce the information regarding redox status through chemosensory pathways. Both PsPto and Dd3937 present chemoreceptors with cytoplasmic domains which could be involved in perception of the energy status driving specific responses during infection. We are working in their characterization through functional and biochemical approaches.

 

Chemosensory signal transduction

While Dd3937 present a unique chemosensory pathway, PsPto encodes four different chemosensory pathways. We are working to understand their role in pathogenesis through the construction and functional characterization of mutant strains altered in different levels of these pathways. Our results point to the existence of a crosstalk among them to regulate pathogenesis-related traits.



Chemosensory cluster in Dd3937



Chemosensory clusters in PsPto

 

In PsPto We have described the effect of blue light on the expression of 5 specific CRs genes during the early stages of PsPto infection, showing that light perception, chemotaxis and virulence are highly interwoven processes.



(Santamaría-Hernando et al., 2020)

 

Ecology of chemoreceptors: a global genomic and metagenomic study

In collaboration with the Comparative Genomics and Metagenomics group of the CBGP leaded by Dr. Jaime Huerta Cepas we are working on the description of the chemoreceptor profiles in different environments from metagenomic data. We are particularly interested in figure out if the bacterial CR profile is a signature of a crop microbiome and therefore if we can predict and diagnose bacterial-plant interactions using CR profiles. With that purpose we are working on a sequence capture methodology to study CRs in crop samples.

 

 

 

Other research lines

MULTILEVEL INTERFERENCE OF SEED TRANSMISSION FOR A SUSTAINABLE MANAGEMENT OF CROP VIRAL DISEASES (SEEDPROTECT). In collaboration with Dr. Israel Pagan and Dr. Fernando García-Arenal from the CBGP, we are analyzing the effect of bacterial and viruses mixed infection on viral seed transmission.


PLANT-PATHOGEN BIOTECHNOLOGY AND GENOMICS MEET FLUID DYNAMICS MIT-UPM seed projects. In collaboration with Dr. Lydia Borouiba from the Massachusetts Institute of Technology, Boston (USA), we are working on the dynamic of bacterial plant infection transmission through the analysis of bacterial dispersion in fluids in the plant environment.

 

Funding

  1. PID2021-125673OB-I00. BACTERIAL CHEMOSENSING IN THE ADAPTATION TO PLANT ENVIRONMENT AND ITS FUNCTION IN PATHOGENESIS (CHEMOADAPT).
    01/09/2022 - 31/08/2025. Ministerio de Ciencia e Innovación/Agencia Estatal de Investigación (MICIN/AEI), Spain. PI: Emilia López Solanilla, Co-PI:José Juan Rodríguez Herva.
  2. PDC2022-133895-I00. EVALUATION OF D-Asp AS A CHEMOTAXIS INTERFERING AGENT FOR THE CONTROL AND PREVENTION OF BACTERIAL PLANT DISEASE (CHEMOINTERFER). 01/12/2022 - 30/11/2024. Ministerio de Ciencia e Innovación/Agencia Estatal de Investigación (MICIN/AEI), Spain. PI: Emilia López Solanilla.
  3. TED2021-130793B-I00. MULTILEVEL INTERFERENCE OF SEED TRANSMISSION FOR A SUSTAINABLE MANAGEMENT OF CROP VIRAL DISEASES (SEEDPROTECT).
    01/12/2022 - 30/11/2024. Ministerio de Ciencia e Innovación/Agencia Estatal de Investigación (MICIN/AEI), Spain. PI: Jesús Israel Pagán, Co-PI: Emilia López Solanilla.
  4. RTI2018-095222-B-I00. RELEVANCE OF CHEMOSENSORY FUNCTIONS DURING THE INFECTION PROCESS OF PHYTOPATHOGENIC BACTERIA (PATOBACTOSENSE).
    01/01/2019 - 31/12/2021 extended until 30/09/2022. Ministerio de Ciencia, Innovación y Universidades/Agencia Estatal de Investigación (MICIN/AEI), Spain. PI: Emilia López Solanilla.
  5. PLANT-PATHOGEN BIOTECHNOLOGY AND GENOMICS MEET FLUID DYNAMICS.
    01/01/2020 - 31/12/2022. MIT-UPM seed projects. Massachusetts Institute of Technology (MIT), Boston, USA.. PI: Emilia López Solanilla, Co-PI: Lydia Borouiba.

 


Representative Publications (last 10 years):

Molina, A., Sánchez-Vallet, A., Jordá, L., Carrasco-López, C., Rodríguez-Herva, J.J., López-Solanilla, E. 2024. Plant cell walls: source of carbohydrate-based signals in plant-pathogen interactions. Current Opinion in Plant Biology 82, 102630. DOI: 10.1016/j.pbi.2024.102630

Munar-Palmer, M., Santamaría-Hernando, S., Liedtke, J., Ortega, D.R., López-Torrejón, G., Rodríguez-Herva, J.J., Briegel, A., López-Solanilla, E. 2024. Chemosensory systems interact to shape relevant traits for bacterial plant pathogenesis. mBio e00871-24. DOI: 10.1128/mbio.00871-24

Rodríguez del Río, Á., Giner-Lamia, J., Cantalapiedra, C.P., Botas, J., Deng, Z., Hernández-Plaza, A., Munar-Palmer, M., Santamaría-Hernando, S., Rodríguez-Herva, J.J., Ruscheweyh, H.-J., Paoli, L., Schmidt, T.S.B., Sunagawa, S., Bork, P., López-Solanilla, E., Coelho, L.P., Huerta-Cepas, J. 2023. Functional and evolutionary significance of unknown genes from uncultivated taxa. Nature 1–3. DOI: 10.1038/s41586-023-06955-z

Gálvez-Roldán, C., Cerna-Vargas, J.P., Rodriguez Herva, J.J., Krell, T., Santamaria-Hernando, S., López-Solanilla, E. 2023. A NIT sensor domain containing chemoreceptor is required for a successful entry and virulence of Dickeya dadantii 3937 in potato plants. Phytopathology®. DOI: 10.1094/PHYTO-10-22-0367-R

Contreras, E., Rodriguez-Herva, J.J., Diaz, I., Lopez-Solanilla, E., Martinez, M. 2023. Previous interaction with phytopathogenic bacteria alters the response of Arabidopsis against Tetranychus urticae herbivory. Journal of Plant Interactions 18, 2144651. DOI: 10.1080/17429145.2022.2144651

Santamaría-Hernando, S., López-Maroto, Á., Galvez-Roldán, C., Munar-Palmer, M., Monteagudo-Cascales, E., Rodríguez-Herva, J.J., Krell, T., López-Solanilla, E. 2022. Pseudomonas syringae pv. tomato infection of tomato plants is mediated by GABA and l-Pro chemoperception. Molecular Plant Pathology 23, 1433–1445. DOI: 10.1111/mpp.13238

Sanchis-López, C., Cerna-Vargas, J.P., Santamaría-Hernando, S., Ramos, C., Krell, T., Rodríguez-Palenzuela, P., López-Solanilla, E., Huerta-Cepas, J., Rodríguez-Herva, J.J. 2021. Prevalence and Specificity of Chemoreceptor Profiles in Plant-Associated Bacteria. mSystems e00951-21. DOI: 10.1128/mSystems.00951-21

Santamaría-Hernando, S., Cerna-Vargas, J.P., Martínez-García, P.M., de Francisco-de Polanco, S., Nebreda, S., Rodríguez-Palenzuela, P., Rodríguez-Herva, J.J., López-Solanilla, E. 2020. Blue-light perception by epiphytic Pseudomonas syringae drives chemoreceptor expression, enabling efficient plant infection. Molecular Plant Pathology 21, 1606–1619. DOI: 10.1111/mpp.13001

Moreno-Pérez, A., Pintado, A., Murillo, J., Caballo-Ponce, E., Tegli, S., Moretti, C., Rodríguez-Palenzuela, P., Ramos, C. 2020. Host Range Determinants of Pseudomonas savastanoi Pathovars of Woody Hosts Revealed by Comparative Genomics and Cross-Pathogenicity Tests. Frontiers in Plant Science 11, 973. DOI: 10.3389/fpls.2020.00973

Cerna-Vargas, J.P., Santamaría-Hernando, S., Matilla, M.A., Rodríguez-Herva, J.J., Daddaoua, A., Rodríguez-Palenzuela, P., Krell, T., López-Solanilla, E. 2019. Chemoperception of Specific Amino Acids Controls Phytopathogenicity in Pseudomonas syringae pv. tomato. mBio 10, e01868-19. DOI: 10.1128/mBio.01868-19

Santamaría-Hernando, S., Senovilla, M., González-Mula, A., Martínez-García, P.M., Nebreda, S., Rodríguez-Palenzuela, P., López-Solanilla, E., Rodríguez-Herva, J.J. 2019. The Pseudomonas syringae pv. tomato DC3000 PSPTO_0820 multidrug transporter is involved in resistance to plant antimicrobials and bacterial survival during tomato plant infection. PLOS ONE 14, e0218815. DOI: 10.1371/journal.pone.0218815

Santamaría‐Hernando, S., Rodríguez‐Herva, J.J., Martínez‐García, P.M., Río‐Álvarez, I., González‐Melendi, P., Zamorano, J., Tapia, C., Rodríguez‐Palenzuela, P., López‐Solanilla, E. 2018. Pseudomonas syringae pv. tomato exploits light signals to optimize virulence and colonization of leaves. Environmental Microbiology 20, 4261–4280. DOI: 10.1111/1462-2920.14331

Castañeda-Ojeda, M.P., Moreno-Pérez, A., Ramos, C., López-Solanilla, E. 2017. Suppression of Plant Immune Responses by the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 Type III Effector Tyrosine Phosphatases HopAO1 and HopAO2. Frontiers in Plant Science 8, 680. DOI: 10.3389/fpls.2017.00680

Bardaji, L., Echeverría, M., Rodríguez-Palenzuela, P., Martínez-García, P.M., Murillo, J. 2017. Four genes essential for recombination define GInts, a new type of mobile genomic island widespread in bacteria. Scientific Reports 7, 46254. DOI: 10.1038/srep46254

Castañeda‐Ojeda, M.P., López‐Solanilla, E., Ramos, C. 2017. Differential modulation of plant immune responses by diverse members of the Pseudomonas savastanoi pv. savastanoi HopAF type III effector family. Molecular Plant Pathology 18, 625–634. DOI: 10.1111/mpp.12420

Martínez‐García, P.M., López‐Solanilla, E., Ramos, C., Rodríguez‐Palenzuela, P. 2016. Prediction of bacterial associations with plants using a supervised machine-learning approach. Environmental Microbiology 18, 4847–4861. DOI: 10.1111/1462-2920.13389

Pérez-Bueno, M.L., Granum, E., Pineda, M., Flors, V., Rodriguez-Palenzuela, P., López-Solanilla, E., Barón, M. 2016. Temporal and Spatial Resolution of Activated Plant Defense Responses in Leaves of Nicotiana benthamiana Infected with Dickeya dadantii. Frontiers in Plant Science 6, 1209. DOI: 10.3389/fpls.2015.01209

Arrebola, E., Carrión, V.J., Gutiérrez-Barranquero, J.A., Pérez-García, A., Rodríguez-Palenzuela, P., Cazorla, F.M., de Vicente, A. 2015. Cellulose production in Pseudomonas syringae pv. syringae: a compromise between epiphytic and pathogenic lifestyles. FEMS Microbiology Ecology 91, fiv071. DOI: 10.1093/femsec/fiv071

Martínez-García, P.M., Ramos, C., Rodríguez-Palenzuela, P. 2015. T346Hunter: A Novel Web-Based Tool for the Prediction of Type III, Type IV and Type VI Secretion Systems in Bacterial Genomes. PLOS ONE 10, e0119317. DOI: 10.1371/journal.pone.0119317

Magno-Pérez-Bryan, M.C., Martínez-García, P.M., Hierrezuelo, J., Rodríguez-Palenzuela, P., Arrebola, E., Ramos, C., de Vicente, A., Pérez-García, A., Romero, D. 2015. Comparative Genomics Within the Bacillus Genus Reveal the Singularities of Two Robust Bacillus amyloliquefaciens Biocontrol Strains. Molecular Plant-Microbe Interactions 28, 1102–1116. DOI: 10.1094/MPMI-02-15-0023-R

Río‐Álvarez, I., Muñoz‐Gómez, C., Navas‐Vásquez, M., Martínez‐García, P.M., Antúnez‐Lamas, M., Rodríguez‐Palenzuela, P., López‐Solanilla, E. 2015. Role of Dickeya dadantii 3937 chemoreceptors in the entry to Arabidopsis leaves through wounds. Molecular Plant Pathology 16, 685–698. DOI: 10.1111/mpp.12227

Tellez-Rio, A., García-Marco, S., Navas, M., López-Solanilla, E., Rees, R.M., Tenorio, J.L., Vallejo, A. 2015. Nitrous oxide and methane emissions from a vetch cropping season are changed by long-term tillage practices in a Mediterranean agroecosystem. Biology and Fertility of Soils 51, 77–88. DOI: 10.1007/s00374-014-0952-5

Martínez-García, P.M., Ruano-Rosa, D., Schilirò, E., Prieto, P., Ramos, C., Rodríguez-Palenzuela, P., Mercado-Blanco, J. 2015. Complete genome sequence of Pseudomonas fluorescens strain PICF7, an indigenous root endophyte from olive (Olea europaea L.) and effective biocontrol agent against Verticillium dahliae. Standards in Genomic Sciences 10, 10. DOI: 10.1186/1944-3277-10-10

Tellez-Rio, A., García-Marco, S., Navas, M., López-Solanilla, E., Tenorio, J.L., Vallejo, A. 2015. N2O and CH4 emissions from a fallow–wheat rotation with low N input in conservation and conventional tillage under a Mediterranean agroecosystem. Science of The Total Environment 508, 85–94. DOI: 10.1016/j.scitotenv.2014.11.041

Santander, R.D., Monte-Serrano, M., Rodríguez-Herva, J.J., López-Solanilla, E., Rodríguez-Palenzuela, P., Biosca, E.G. 2014. Exploring new roles for the rpoS gene in the survival and virulence of the fire blight pathogen Erwinia amylovora. FEMS Microbiology Ecology 90, 895–907. DOI: 10.1111/1574-6941.12444

Taurino, M., Abelenda, J.A., Río‐Alvarez, I., Navarro, C., Vicedo, B., Farmaki, T., Jiménez, P., García‐Agustín, P., López‐Solanilla, E., Prat, S., Rojo, E., Sánchez‐Serrano, J.J., Sanmartín, M. 2014. Jasmonate-dependent modifications of the pectin matrix during potato development function as a defense mechanism targeted by Dickeya dadantii virulence factors. The Plant Journal 77, 418–429. DOI: 10.1111/tpj.12393

Río‐Álvarez, I., Rodríguez‐Herva, J.J., Martínez, P.M., González‐Melendi, P., García‐Casado, G., Rodríguez‐Palenzuela, P., López‐Solanilla, E. 2014. Light regulates motility, attachment and virulence in the plant pathogen Pseudomonas syringae pv tomato DC3000. Environmental Microbiology 16, 2072–2085. DOI: 10.1111/1462-2920.12240