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Biology of beneficial plant-microorganism interactions

Specialized Group:

Biology of beneficial plant-microorganism interactions

Department of Microbiology of the Faculty of Biology of the University of Seville. Avda.de Reina Mercedes 6, 41012-Seville.

Currently, within the research group there are six members who act as principal investigators and who belong to the PAIDI group of the Junta de Andalucía, BIO-169: José María Vinardell González, Francisco Javier López Baena, Carlos Medina Morillas, Patricia Bernal Guzmán (> see moreCurrently, within the research group there are six members who act as principal investigators and who belong to the PAIDI group of the Junta de Andalucía, BIO-169: Jose Manuel Borrero de Acuña (> see more) Y Francisco Pérez Montaño (> see more).

The research group studies various rhizobacteria that promote the growth of plants of agricultural interest through biofertilization, biostimulation and / or biocontrol. We mainly investigate the molecular signals that govern the symbiotic N-binding interaction.2 Currently, within the research group there are six members who act as principal investigators and who belong to the PAIDI group of the Junta de Andalucía, BIO-169:

We use the models: a) Sinorhizobium fredii–Soy, b) Rhizobium tropics–bean, c) Sinorhizobium meliloti-alfalfa, and d) Pseudomonas putida-phytopathogens.

Our objective is to generate knowledge that contributes to sustainable agriculture and its adaptation to adverse environments, in order to generate alternatives and thus avoid, or at least reduce, the use of chemical fertilizers and pesticides.

Below are the components of the PAIDI group in alphabetical order:

BIO169Below are the components of the PAIDI group in alphabetical order:

o Azogue Palma, Carlos – Hired project intern

o Ayala García, Paula – FPU predoctoral fellow

o Bernal Guzmán, Patricia – Hired Ramón y Cajal

o Borrero de Acuña, José Manuel – Hired Emergia

o Buendía Clavería, Ana María – University Professor

o Cubo Sánchez, María Teresa – University Professor

o Del Cerro Sánchez, Pablo – Hired Ramón y Cajal

o Espuny Gómez, María del Rosario – University Professor

o Fuentes Romero, Francisco – Junta de Andalucía predoctoral fellow

o García Rodríguez, Diego – PIF predoctoral fellow

o Herrero Gómez, Irene – FPU predoctoral fellow

o Jacott, Catherine Nancy – Researcher Juan de la Cierva training

o Jiménez Guerrero, Irene – Researcher Juan de la Cierva incorporation

o López Baena, Francisco Javier – Full University Professor

o Medina Morillas, Carlos – University Professor

o Moreno de Castro, Natalia – FPU predoctoral fellow

o Ollero Márquez, Francisco Javier – University Professor

o Pérez Montaño, Francisco – Full University Professor

o Reyes Pérez, Pedro José – Predoctoral fellow hired as a project

or Vinardell Gonzalez, Jose Maria – University Professor

Joseborrero
Engineering extracellular membrane vesicles from rhizospheric bacteria for the development of biopesticides and plant-growth promoting agents
Engineering of extracellular membrane vesicles of rhizospheric bacteria for the development of biopesticides and plant growth promoting agents

PI: Jose Manuel Borrero de Acuña

Research in our lab:

One of our major endeavours is to elucidate protein complex assembly dynamics involved in crucial biological processes for diverse bacteria. The majority of cellular functions in all living cells are conducted by proteins. Biochemical pathways, signal transduction cascades, and membrane-associated complexes of energy generation rely on the fine-tuned, directed and frequently transient protein interactions. We have widely investigated biochemical processes for relevant human pathogens (Legionella pneumophila, Clostridioides difficile and P. aeruginosa) and environmentally relevant bacteria (Dinoroseobacter shibae and Pseudomonas putida); (see publications: https://scholar.google.es/citations?user=lo_iLZQAAAAJ&hl=es&oi=ao). Dissecting the protein-protein interactions underlying such processes is crucial for basic research but it is also a cornerstone for boundless biomedicine and biotechnological applications. We also investigate the molecular processes governing organisms’ interactions in their natural niche. Our interest is drawn towards the elucidation of the biogenesis pathways and cell-to-cee communication mechanisms driven by extracellular membrane vesicles (EMVs). EMVs are nanoparticles involved in a broad range of biological processes including horizontal DNA transfer, decoy for phages and antibiotics, disposal of waste material and surface remodeling, nutrient scavenging, bacterial killing, host response immunomodulation and delivery of bioactive compounds and thus are essential for inter- intra-species and inter-kingdom communication. Recently, interactomic-driven research has led us to the identification of highly conserved proteins sustaining EMV formation across species. In our current projects we propose to exploit the full potential of EMVs for the benefit of bacteria-plant interactions. To this end, we employ interactomics techniques consisting of affinity purification coupled with mass spectrometry, SPOT-membrane arrays, immunofluorescence and immunogold labelling microscopy and others to identify further protein-protein interactions underlying the biogenesis of EMVs in different bacterial species present in the plant holobiont. We induce the expression of these proteins found in the interactomic studies to modulate vesicle formation rate, size and amount. We intend to tailor the protein and metabolic cargo of EMVs by encapsulating nodulation factors, plant-priming molecules, nitrogen nitrogen-fixing enzymes or phytopathogen inhibitors. Thereby, EMVs can be used as organism-free biopesticides for phytopathogen killing or as bioinoculants to enhance nodulation, nitrogen fixation and ultimately plant growth. Nonetheless, EMV research go beyond the applications related to sustainable agriculture since novel molecular tools arising from this work can be applied in multiple disciplines, ranging from biomedicine (development of vaccines) to bioremediation (design of EMV-based xenobiotic degraders).

 

Research lines in our laboratory:
Our group is extensively focused on elucidating the assembly dynamics of protein complexes involved in crucial biological processes for various bacteria. Most cellular functions in all living cells are carried out by proteins. Biochemical pathways, signal transduction cascades, and membrane-associated energy-generating complexes depend on directed and often transient protein interactions. We extensively investigated the biochemical processes of relevant human pathogens (Legionella pneumophila, Clostridioides difficile, and Pseudomonas aeruginosa) and environmentally important bacteria (Dinoroseobacter shibae and Pseudomonas putida); (see publications: https://scholar.google.es/citations?user=lo_iLZQAAAAJ&hl=es&oi=ao). Dissecting the protein-protein interactions underlying such processes is crucial for basic research, but is also a pillar for multiple biomedical and biotechnological applications. We also investigate the molecular processes that govern the interactions of organisms in their natural niche. Our interest focuses on the elucidation of biogenesis pathways and cell-to-cell communication mechanisms driven by extracellular membrane vesicles (EMVs). VEMs are nanoparticles that are involved in a wide range of biological processes, such as horizontal DNA transfer, decoy function for phages and antibiotics, waste material removal and surface remodeling, nutrient removal, bacteria, immunomodulation of the host response and delivery of bioactive compounds, making them essential for communication between species and between kingdoms. Recently, our interactomics-based research has led us to the identification of highly conserved proteins that underpin the formation of VEMs across species. Currently, we propose to exploit the full potential of VEMs for the benefit of bacteria-plant interactions. To this end, we use interactomics techniques consisting of purification by affinity chromatography coupled to mass spectrometry, SPOT membrane matrices, immunofluorescence microscopy and immunolabeling with gold particles, among others, to identify other protein-protein interactions underlying the biogenesis of VEMs in different bacterial species present in the holobiont. Next, we induce the expression of these proteins found in the interactomic studies to modulate the rate, size and amount of vesicle formation. We intend to adapt the protein and metabolic load of the VEMs by encapsulating nodulation factors, molecules for the “vaccination” of plants, nitrogen-fixing enzymes or phytopathogen inhibitors. Thus, VEMs can be used as biopesticides to eliminate phytopathogens or as bioinoculants to improve nodulation, nitrogen fixation and, ultimately, plant growth. However, VEM research goes beyond applications related to sustainable agriculture, since the new molecular tools derived from this work can be applied in multiple disciplines, ranging from biomedicine (vaccine development) to bioremediation ( design of xenobiotic degraders based on VEMs).
The following techniques are available in our lab:

Figure 1. General interactomic workflow. The illustration depicts step by step the protein–protein interaction elucidation pathway via affinity chromatography copurification coupled with mass spectrometry (Borrero de Acuña, J. M. et al 2017).

 

Figure 2. Experimental workflow designed for the isolation and characterisation of extracellular membrane vesicles (EMVs). (1) Growth of bacterial culture under standard conditions to produce EMVs. (2) Harvesting of cells and filtering of supernatants to remove remaining cells. (3) Ultrafiltration to remove impurities and concentrate EMV fractions. (4) Ultracentrifugation to collect EMV fractions. (5) Evaluation of the EMVs structure and integrity by electron microscopy. (6) Quantification of EMVs using scattering-light reliant Nanosight technology. Abbreviations: EMVs = extracellular membrane vesicles.

 

 

Research projects

  • Title: Engineering extracelular membrane vesicles from rhizospheric bacteria for the development of biopesticides and plant-growth promoting agents.
    • Funding Entity: Projects of Excellence 2021. General Secretariat of Universities, Research and Technology, Junta de Andalucía.
    • Reference: ProyExcel_00450 Affiliation: Sevilla University Duration: December 2022-November 2025
    • Funding Granted: 140.937,14€ Principal Investigator: Dr Jose Manuel Borrero de Acuña & Dr. Patricia Bernal
  • Title: Development of biopesticides based on membrane vesicles as a sustainable alternative to polluting chemical pesticides.
    • Funding Entity: Ministry of Science and Innovation, Strategic Projects Oriented to the Ecological Transition and the Digital Transition 2021, Government of Spain
    • Reference: TED2021-130357B-I00 Affiliation: Sevilla University Duration: December 2022-November 2024
    • Funding Granted: 253.000,00€ Principal Investigator : Dr Jose Manuel Borrero de Acuña & Dr. Patricia Bernal
  • Title: Enhancing the symbiotic cross-talk through rhizobial membrane vesicles.
    • Funding Entity: Ministry of Science and Innovation, Knowledge Generation Projects 2021, Government of Spain
    • Reference: PID2021-122395OA-I00 Affiliation: Sevilla University Duration: September 2022-August 2026
    • Funding Granted: 145.200,00€ Principal Investigator: Dr Jose Manuel Borrero de Acuña
  • Title: Engineering membrane vesicles for fine-tuned modulation of rhizobia species interactions for enhanced nodulation and plant growth.
    • Funding Entity: Junta de Andalucía, Ministry of economic transformation, industry, knowledge and universities
    • Reference: EMERGIA20_00048 Affiliation: Sevilla University
    • Duration: November 2021- August 2025 Principal Investigator: Dr Jose Manuel Borrero de Acuña
  • Title: Developing a rodent disease model for Pseudomonas aeruginosa infection in bronchiectasis for drug research.
    • Funding Entity: Federal Ministry of Education and Research (Germany)
    • Reference: 281361126/GRK2223 Affiliation: Technical University Braunschweig
    • Duration: December 2020- November 2023 Principal Investigator: Dr Jose Manuel Borrero de Acuña
Pat
Selected publications
  • Jiménez-Guerrero, I., López-Baena, F.J., Borrero-de Acuña, J.M.* & Pérez-Montaño, F. (2023). Membrane vesicle engineering with “à la carte” bacterial-immunogenic molecules for
    organism-free plant vaccination. Microbial Biotechnology, (accepted; ahead of print). *Corresponding author
  • Borrero-de Acuña, J.M., & Poblete‐Castro, I.* (2023). Rational engineering of natural polyhydroxyalkanoates producing microorganisms for improved synthesis and
    recovery. Microbial Biotechnology, 16(2), 262-285.
  • Michel, A. M., Borrero-de Acuña, J. M.*, Molinari, G., … & Jahn, D. (15 authors); (2022).Cellular adaptation of Clostridioides difficile to high salinity encompasses a compatible solute‐
    responsive change in cell morphology. Environmental Microbiology, 24(3), 1499-1517.*Corresponding author
  • Borrero de Acuña, J.M., & Bernal, P.*; (2021). Plant holobiont interactions mediated by the type VI secretion system and the membrane vesicles: promising tools for a greener
    agriculture. Environmental Microbiology, 23(4), 1830-1836.
  • Borrero-de Acuña, J.M., Gutierrez-Urrutia, I., Hidalgo-Dumont, C., … & Poblete‐Castro, I.*; (14 authors); (2020). Channelling carbon flux through the meta‐cleavage route for improved
    poly (3‐hydroxyalkanoate) production from benzoate and lignin‐based aromatics in Pseudomonas putida H. Microbial Biotechnology 14(6), 2385-2402.
  • Borrero-de Acuña, J.M., & Poblete-Castro, I.*; (2020). Expanding the Reach of Recombineering to Environmental Bacteria. Trends in Biotechnology, 38(7):684-685.
  • Poblete-Castro, I., Aravena-Carrasco, C., Orellana-Saez, M., Pacheco, N., Cabrera, A., & Borrero-de Acuña, J.M.*; (2020). Engineering the osmotic state of Pseudomonas putida
    KT2440 for efficient cell disruption and downstream processing of poly (3-hydroxyalkanoates). Frontiers in Bioengineering and Biotechnology, 8: 161. *Corresponding author
  • Borrero-de Acuña, J.M.*, Timmis, KN, Jahn, M. & Jahn, D. (2017). Protein complex formation during denitrification by Pseudomonas aeruginosa. Microbial Biotechnology, 10(6),
    1523-1534. *Corresponding author
  • Borrero-de Acuña, J.M.*, Hidalgo-Dumont, C., Pacheco, N., Cabrera, A. & Poblete-Castro, I.* (2017). A novel programmable lysozyme-based lysis system in Pseudomonas
    putida for biopolymer production. Scientific Reports, 29;7(1): 4373. *Co-Corresponding authors
  • Borrero-de Acuna, J.M., Rohde, M., Wissing, J., … & Jahn, D.*; (9 authors). (2016) Protein network of the Pseudomonas aeruginosa denitrification apparatus. Journal of
    Bacteriology. 198(9): 1401-13

 

PhD students
  • Irene Herrero Gómez: Enhancing the symbiotic cross-talk through rhizobial membrane vesicles.
  • Natalia Moreno de Castro: Engineering membrane vesicles for fine-tuned modulation of rhizobia species interactions for enhanced nodulation and plant growth.
  • Carlos Azogue Palma: Engineering membrane vesicles for efficient production of industrially valuable chemicals.
Riga Bernal

 

 

 

The type VI secretion system (T6SS) of Pseudomonas putida. Powerful biocontrol weapon for the protection of crops of interest

IP: Patricia Bernal

Dr. Bernal's line of research focuses on the study of Type VI Secretion Systems (T6SS) in Pseudomonas putida. P. putida it is a soil bacterium with the ability to colonize the roots of different crop plants providing growth advantages and at the same time protection against pathogens; therefore this strain is considered an excellent agent of biological control (biocontrol). Biocontrol of diseases caused by plant pathogens is considered an excellent alternative to chemical pesticides to protect our crops, since these can cause contamination of the subsoil and the loss of the natural microbiota of both the soil and the plant. For this reason, the funding agencies have prioritized different initiatives aimed at promoting more sustainable agriculture, including biocontrol. To progress in this field of research, it is key to understand in a comprehensive and complete way the molecular mechanisms of biological control carried out by known and well-established biocontrol agents such as Pseudomonas putida.

In P. putida, the T6SS has recently been established as a important biocontrol mechanism which gives this strain almost all of its biocontrolling capacity (Bernal et al. 2017). The T6SS is considered a powerful antibacterial weapon and P. putida uses it efficiently to kill extremely deleterious plant pathogens such as Pseudomonas syringae O Agrobacterium tumefaciens. P. putida It contains three T6SSs called K1-, K2-, and K3-T6SS. K1-T6SS is induced in a stationary growth phase, secretes toxins and kills a wide range of phytopathogenic bacteria such as P. syringae, Xanthomonas campestris O Agrobacterium tumefaciens (Bernal et al. 2017, Bernal et al. 2021). This antimicrobial capacity against phytopathogens has been observed both in experiments in vitro as in experiments in planta (Bernal et al. 2017, Bernal et al. 2021).

At a structural level, T6SS is a contractile nanomachine made up of a membrane component, a tail (contractile tube and sheath) and a base plate. The membrane component anchors the system to the cell envelope that brings together the base plate components from where the glue polymerizes. Once the system is assembled, the sheath contracts and the tube with the effector proteins is ejected into the target cells (Fig. 3). An elemental component of this system, the TssA protein, is essential for the assembly of the sheath. Despite their key function, TssA proteins exhibit unexpected diversity and exist in two main forms, a short form (TssAS) and a long form (TssAL). While the TssA proteinsL interact with the TagA protein to anchor the distal end of the extended sheath, the stabilization mechanism of T6SS containing TssAS it was still unknown. In a recent study (Bernal et al., 2021) we have identified a new category of structural components (TagB and TagJ proteins) that interact with TssA proteinss and contribute to the assembly of the T6SS by stabilizing the polymerized sheath from the base plate. In addition, we have shown that the presence of these components is important for full extension of the sheath and for maintaining optimal firing ability. Likewise, it has been seen that the association of different forms of TssA proteins with a different class of sheath stabilizing proteins results in T6SS that reside well in the cell for some time (TssAL-TagA) or fire immediately after extension of the sheath (TssAS-TagB). It is proposed that this diversity in shooting dynamics could contribute to the specialization of T6SS to adapt to different bacterial lifestyles in various environmental niches (Bernal et al., 2021).

The lines of research carried out in Dr. Bernal's laboratory are aimed at learning more about the function and mechanism of action of these antimicrobial systems, allowing them to be adapted to develop highly effective biocontrol agents that are more specific and with greater power to eradicate plant pathogens and be a tool for future biotechnological applications applied to agriculture.

This video summarizes the project financed by the BBVA Foundation between 2021-2022 and entitled: The biocontrol super agent Pseudomonas putida KT2440 as a sustainable measure to fight against Xylella fastidiosa, the great threat to our olive grove

Active projects
  • Title of the project: Engineering extracelular membrane vesicles from rhizospheric bacteria for the development of biopesticides and plant-growth promoting agents.
    • Financing entity: Projects of Excellence 2021. General Secretariat of Universities, Research and Technology, Junta de Andalucía.
    • Reference: ProyExcel_00450 Lead Entity: Sevilla University Period: December 2022-November 2025
    • Subsidy amount: 140.937,14€ Responsible Researcher: Dr. Patricia Bernal & Jose Manuel Borrero de Acuña
  • Title of the project: Development of biological pesticides based on membrane vesicles as a sustainable alternative to highly polluting chemical pesticides (BIOPESTOMV).
    • Financing entity: Ministry of Science and Innovation, Strategic Projects Oriented to the Ecological Transition and the Digital Transition 2021, Government of Spain
    • Reference: TED2021-130357B-I00 Lead Entity: Sevilla University Period: December 2022-November 2024
    • Subsidy amount: 253.000,00€ Responsible Researcher: Dr. Patricia Bernal & Jose Manuel Borrero de Acuña
  • Title of the project: Optimizing Pseudomonas putida as a crop protection agent: environmental signals, specificity and efficiency of the type vi secretion system as a biocontrol weapon
    • Financing entity: Ministry of Science and Innovation, Knowledge Generation Projects 2021, Government of Spain
    • Reference: PID2021-123000OB-I00 Lead Entity: Sevilla University Period: September 2022-August 2025
    • Subsidy amount: 175.450,00€ Responsible Researcher: Dr. Patricia Bernal
  • Title of the project: Biological control studies for crop protection through the use of the bacterial type VI secretion system (T6SS)
    • Financing entity: Ministry of Science, Innovation and Universities, Ramón y Cajal Program Call 2019, Government of Spain
    • Reference: RYC2019-026551-I Lead Entity: Sevilla University
    • Period: April 2021-March 2026 Responsible Researcher: Dra. Patricia Bernal
Featured posts
  • Bernal, P*, Civantos, C, Pacheco-Sánchez, D, Quesada, JM, Filloux, A*, and Llamas*, MA (2023). Transcriptional organization and regulation of the Pseudomonas putida K1 Type VI secretion system gene cluster. Microbiology 169:001295. (*Co-author of correspondence).
  • González-Magaña, A, Altuna, J, Queralt-Martín, M, Largo, E, Velázquez, C, Montánchez, I, Bernal, P, Alcaraz, A, Albesa-Jové, D (2022). The P. aeruginosa effector Tse5 forms ion-selective membrane pores that disrupt the membrane potential of intoxicated bacteria. Communications Biology. 5:1189.
  • Bernal, P*, Eberl, L., Young, R., Lepek, V.C. & Malone, J.G. (2021) Understanding plant-microorganism interactions to envision a future of sustainable agriculture. Editorial. Environ Microbiol. 23: 1809-1811 (* Author of correspondence).
  • Borrero de Acuña, JM, & Bernal, P* (2021). Plant holobiont interactions mediated by the type VI secretion system and the membrane vesicles: promising tools for a greener agriculture. Environ Microbiol. 23: 1830-1836 (* Author of correspondence).
  • Duran, D, Bernal, P, David Vazquez-Arias, Blanco-Romero, E, Garrido-Sanz, D, Redondo-Nieto, M, Rivilla, R and, Martin, M. (2021). Pseudomonas fluorescens F113 type VI Secretion Systems mediate bacterial killing and adaption to the rhizosphere microbiome. Scientific Report 11:5772-5785.
  • Bernal, P, Furniss, CD, Fecht, S, Leung, RCY, Spiga, L, Mavridou, DAI & Filloux. (2021). A novel stabilization mechanism for the type VI secretion system sheath. Proc Natl Acad Sci. 118:e2008500118
  • Bernal, P, Murillo-Torres, M & Allsopp, LP (2020). Integrating signals to drive T6SS killing. Environ Microbiol 22:4520-4523.
  • Allsopp, LP, Bernal, P, Nolan, L & Filloux A. (2020). Causalities of War: The connection between T6SS & microbiota. Cell Microbiol 22:e13153.
  • Bernal, P. *, Llamas, MA, Filloux, A. (2018). Type VI secretion Systems in plant-associated bacteria. Environ Microbiol 20: 1-15 (* Correspondence author).
  • Bernal, P. *, Allsopp, L.P., Filloux, A., and Llamas M.A. (2017). The Pseudomonas putida T6SS is a plant warden against phytopathogens. ISME Journal 11: 972-987 (* Author of correspondence).
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Role of the type VI secretion system and external membrane vesicles in the rhizobia-legume interaction.
IP: Francisco Pérez Montaño

Our research group aims to delve into the mechanisms that determine the specificity and efficiency of nodulation mediated by the type VI secretion system in rhizobia, using as a model organism Sinorhizobium fredii USDA257, a strain with one of the largest known host ranges. Furthermore, this project aims to determine the role of this protein secretion system in competition with other rhizospheric bacteria, including some phytopathogenic ones. The expected results of this project will improve the existing knowledge about the mechanisms responsible for rhizobia-legume compatibility, as well as the possible use of rhizobia not only as biofertilizing agents but also as biocontrol agents.

Furthermore, in collaboration with Dr. Borrero de Acuña, our group proposes taking advantage of the full potential of external membrane vesicles for the benefit of rhizobia-legume interactions through a biotechnological approach that avoids the use of GMOs. To do this, in addition to determining the protein and metabolic charge of the external membrane vesicles in different rhizobacteria (St. Fredii HH103 and Rhizobium tropics CIAT 899) and symbiotic stages, the aim is to partially adapt the protein and metabolic load of these membranous structures so that they mostly encapsulate molecules of biotechnological interest, such as nodulation factors, phytohormones, etc. In this way, the final objective is to improve nitrogen fixation and plant growth through the use of vesicles loaded on demand, without the need to use the entire microorganism.

 

Active projects

Title of the project: Antibiosis or symbiosis? Characterizing the type VI secretion system of Sinorhizobium fredii USDA257.

Financing entity: State Plan 2017-2020 Challenges – R&D&i projects. Ministry of Science and Innovation

Reference: PID2020-118279RA-I00 Lead Entity: Sevilla University Period: September 2021-August 2024

Grant Amount: 157.200 € Responsible Researcher: Francisco Pérez Montaño

 

Title of the project: Legumes in biodiversity-based farming systems in Mediterranean basin.

Financing entity: Partnership for Research and Innovation in the Mediterranean Area (PRIMA)

Reference: 2019-SECTION2-19 Lead Entity: IFAPA Center Period: December 2020-November 2023

Grant Amount: 150.000 € Responsible Researcher: Sweet Name Rodríguez Navarro

 

Publications last 5 years (*Preferred authorship)

Jiménez-Guerrero I, López-Baena, FJ, Borrero-de Acuña, JM, Pérez-Montaño F*. (2023). Membrane vesicle engineering with «à la carte» bacterial-immunogenic molecules for organism-free plant vaccination. Microbial Biotechnology. 10.1111/1751-7915.14323

Fuentes-Romero F, Moyano-Bravo I, Ayala-Garcia P, Rodriguez-Carvajal MA, Pérez-Montaño F, Acosta-Jurado S, Ollero FJ, Vinardell JM. (2023). Non-Ionic Osmotic Stress Induces the Biosynthesis of Nodulation Factors and Affects Other Symbiotic Traits in Sinorhizobium fredii HH103. 10.3390/biology12020148.

Ayala-García P, Jiménez-Guerrero I, Jacott CN, López-Baena FJ, Ollero FJ, Del Cerro P, Pérez-Montaño F*. (2022). The Rhizobium tropics CIAT 899 NodD2 protein promotes symbiosis and extends rhizobial nodulation range by constitutive nodulation factor synthesis. 10.1093/jxb/erac325.

de la Osa C, Perez‐Lopez J, Fair AB, Baena G, Marino D, Coleto I, 2005; Pérez-Montaño F, Gandullo J, Echeverria C, García-Nauriño S, Monreal, J. A. (2022). Knock‐down of phosphoenolpyruvate carboxylase 3 negatively impacts growth, productivity and responses to salt stress in sorghum (Sorghum bicolor L.). 10.1111/tpj.15789.

Fuentes-Romero F, Navarro-Gómez P, Ayala-García P, Moyano-Bravo I, López-Baena FJ, Pérez-Montaño F, Ollero FJ, Acosta-Jurado A, Vinardell, J.M. (2022). The noD1 Gene of Sinorhizobium fredii HH103 Restores Nodulation Capacity on Bean in a Rhizobium tropics CIAT 899 nodD1/nodD2 Mutant, but the Secondary Symbiotic Regulators nolR, nodD2 or syrM Prevent HH103 to Nodulate with This Legume. Microorganisms. 10.3390/microorganisms10010139.

Jiménez-Guerrero I, Moreno-de Castro N, Pérez-Montaño F*. (2021). One door closes, another opens: when nodulation impairment with natural hosts extends rhizobial host-range. Environmental Microbiology. 10.1111/1462-2920.15353.

Aharon E; Mookherjee A; Pérez-Montaño F; Mateus da Silva G; Sathyamoorthy R; Burdman, S; Jurkevitch E. (2021). Secretion systems play a critical role in resistance to predation by Bdellovibrio bacteriovorus. Research in Microbiology. 10.1016/j.resmic.2021.103878.

del Cerro P, Ayala-García P, Buzón P, Castells-Graells R, López-Baena FJ, Ollero FJ, Pérez-Montaño F*. (2019). OnfD, an AraC-type transcriptional regulator of Rhizobium tropics CIAT 899 involved in Nod factor synthesis and symbiosis. Applied and Environmental Microbiology. 10.1128/aem.01297-20.

Jiménez-Guerrero I, Acosta-Jurado S, Medina C, Ollero FJ, Alias-Villegas C, Vinardell JM, Pérez-Montaño F, López-Baena FJ. (2020). The Sinorhizobium fredii HH103 Type III secretion system effector NopC blocks nodulation with Lotus japonicus Gifu. Journal of Experimental Botany. 10.1093/jxb/eraa297.

Martinelli F, Ollero FJ, Giovino A, Perrone A, Bekki A, Sikora S, Nabbout RE, Bouhadida M, Yucel D, Bazzicalupo M, Mengoni A, Pérez-Montaño F*. (2020). Proposed research for innovative solutions for chickpeas and beans in a climate change scenario: the Mediterranean Basin. Sustainability. 10.3390/su12041315.

Acosta-Jurado S, Alías-Villegas C, Almozara A, Espuny MR, Vinardell JM, Pérez-Montaño F*. (2020). Deciphering the symbiotic significance of quorum sensing systems of Sinorhizobium fredii HH103. Microorganisms. 10.3390/microorganisms8010068.

Jiménez-Guerrero I, Pérez-Montaño F*, da Silva GM, Wagner N, Shkedy D, Zhao M, Pizarro L, Bar M, Walcott R, Sessa G, Pupko T, Burdman S. (2019). Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III-secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus. Molecular Plant Pathology. 10.1111/mpp.12877.

Yang R, Santos-Garcia D, Pérez-Montaño F, Zhao M, Jimenez-Guerrero, I, Da Silva GM, Rosenberg T, Chen G, Plaschkes I, Morin S, Walcott R, Burdman S. (2019). Complete assembly of the genome of an Acidovorax citrulli strain reveals a naturally occurring plasmid in this species. Frontiers in Microbiology. 10.3389/fmicb.2019.01400.

del Cerro P, Ayala-García P, Jiménez-Guerrero I, López-Baena FJ, Vinardell JM, Megías M, Hungria M, Gil-Serrano A, Pérez-Montaño F, Ollero FJ. (2019). The non-flavonoid inducible nodA3 and the flavonoid regulated nodA1 genes of Rhizobium tropics CIAT 899 guarantee nod factor production and nodulation of different host legumes. Plant and Soil. 10.1007/s11104-019-04073-2.

del Cerro P, Megias M, López-Baena FJ, Gil-Serrano A, Perez-Montano F, Ollero FJ. (2019). Osmotic stress activates nif and fix genes and induces the Rhizobium tropics CIAT 899 Nod factor production via NodD2 by up-regulation of the nodA2 operon and the nodA3 gene. PLoS ONE. 10.1371/journal.pone.0213298.

PhD students in training

Irene Herrero Gómez: Enhancing symbiotic dialogue through rhizobial outer membrane vesicles. Co-supervised with Dr. Borrero de Acuña.

Natalia Moreno de Castro: Engineering of rhizobial outer membrane vesicles for the improvement of nodulation and plant growth. Co-supervised with Dr. Borrero de Acuña.

Paula Ayala García: Dual study of the molecular and physiological mechanisms responsible for nodulation between Rhizobium tropics CIAT 899 and legumes Phaseolus vulgaris and Lotus japonicus. Co-supervised with Dr. Ollero Márquez.

 

Graduated doctoral students

Pablo del Cerro Sánchez: “Gene characterization Rhizobium tropics CIAT899 involved in the biosynthesis of nodulation factors independent of activation by flavonoids and induced by osmotic stress”. 2019. Co-supervised with Dr. Ollero Márquez.
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