Carlos Frey

@unileon.es

Área de Fisiología Vegetal, Departamento de Ingeniería y Ciencias Agrarias, Facultad de Ciencias Biológicas y Ambientales
Universidad de León

Carlos Frey


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https://researchid.co/carlosfrey

EDUCATION

Degree in Biology, Universidad de León, Spain (from 2014 to 2018).
Master's Degree in Research in Fundamental Biology and Biomedicine, Universidad de León, Spain (from 2018 to 2019).
PhD Programme in Molecular Biology and Biotechnology, Universidad de León, Spain (2019 to 2023).
15

Scopus Publications

129

Scholar Citations

6

Scholar h-index

5

Scholar i10-index

Scopus Publications

  • Biochemical diversity of macroalgal cell walls: Insights into the polysaccharide matrix
    Carlos Frey, Jorge Peláez, Antonio Encina, Hugo Mélida
    Algal Research, 2026
  • Cell Wall Dynamics in Haustorial Development of Cuscuta campestris During Parasitism on Differentially Susceptible Hosts
    Carlos Frey, Lucía López-López, Andrea Martínez-Toral, Diego Castro, José Luis Acebes
    International Journal of Molecular Sciences, 2026
    Dodder (Cuscuta campestris) is a parasitic plant that causes severe economic losses to crops such as mung bean (Vigna radiata), although some species, including tomato (Solanum lycopersicum), exhibit varying degrees of resistance. Dodder parasitism begins with the development of the haustorium, whose endophytic primordium undergoes intrusive growth to penetrate host tissues. While the cell walls of endophytic cells are essential for invasion, the sequential changes occurring in these cell walls are not fully understood. This study aims to characterize cell wall modifications in Cuscuta campestris haustoria during parasitism of a susceptible host (Vigna radiata) and a resistant host (Solanum lycopersicum ‘Minibel’), using histochemical and immunohistochemical approaches focused on homogalacturonan (HG) and arabinogalactan proteins (AGPs). In both hosts, AGPs and HG (predominantly in their demethylesterified form) increased in the host-facing epidermal walls, the aligned file cells of the haustoria, and the boundary layer surrounding the haustorial cone. The boundary layer was enriched in AGPs and initially showed massive HG deposition, later incorporating lignin and callose. In tomato, lignin-based resistance was associated with the outermost cortical cells and did not substantially affect the overall dynamics of the dodder cell walls. These findings highlight the central role of coordinated cell wall remodeling in dodder invasion and reveal broadly similar developmental trajectories of HG and AGPs in haustoria formed on susceptible and resistant hosts.
  • The role of plant cell walls in pest resistance: current insights and future perspectives
    Marta Marina Perez-Alonso, Lucia Talavera-Mateo, Dairon Ojeda-Martinez, Laura Barcenilla-Valcárcel, Álvaro Montesinos, et al.
    Journal of Experimental Botany, 2025
    Significant strides have been made by researchers aiming to understand the crucial role of the plant cell wall (PCW) in defending against pathogens. Numerous reviews have synthesized findings on plant–pathogen interactions, shedding light on the role of the PCW in defence, the generation of cell wall damage-associated molecular patterns (DAMPs), perception, and signalling response. However, the role of the PCW in responses to herbivory remains underexplored. This review aims to fill this gap, offering a comprehensive analysis of the current knowledge in this area. For the first time, it consolidates studies focusing on the involvement of the PCW in pest response. The review examines key aspects, including the structural changes in the PCW following pest infestation, the role of cell wall-derived DAMPs, and the phenotypic traits of transgenic plants with modified cell wall components. Additionally, it delves into the genetic underpinnings of cell wall plasticity and the mechanisms of DAMP perception. Lastly, the article identifies promising research pathways to further unravel the complex role of the PCW in pest defence, encouraging advancements in this relatively nascent field. Through this effort, it aims to bridge the knowledge gap and inspire deeper investigations into the interplay between the PCW and pest resistance.
  • Photosynthesis and stress tolerance: cell walls at the cross-roads
    María José Clemente-Moreno, Carlos Frey, Lidia López-Serrano, José Luis Acebes, Jaume Flexas, et al.
    Journal of Experimental Botany, 2025
    The cell wall (CW) plays a pivotal role in plant responses to abiotic stress and the regulation of photosynthesis. Modifications in CW composition and structure can enhance drought tolerance and other stress responses, but often at the expense of photosynthetic efficiency. This review explores the complex relationship between the CW, photosynthesis, and stress tolerance. We describe how changes in CW composition, such as variations in pectin, hemicellulose, and lignin contents, affect CO2 diffusion and, consequently, mesophyll conductance (gm), but also their known effects driving stress tolerance through mechanisms such as altered cell wall elasticity and water retention, and signalling stress response pathways. New analytical and molecular tools offer an unprecedented set of possibilities to develop biotechnological strategies for sustainable agriculture. We conclude that the CW represents a promising target for crop improvement through genetic engineering and ecophysiological studies, but further research is needed to fully understand the underlying mechanisms and avoid unintended effects on photosynthesis and growth.
  • Harnessing macroalgal cell walls to trigger immunity in Arabidopsis thaliana
    Jorge Peláez, Carlos Frey, Diego Rebaque, Francisco Vilaplana, Antonio Encina, et al.
    Plant Stress, 2025
  • Deciphering Antioxidant Responses in Tomato Autografts
    Carlos Frey, Andrés Hernández-Barriuso, José Luis Acebes, Antonio Encina
    Antioxidants, 2025
    Grafting is a horticultural technique that involves a healing process that requires grafted plants to develop physiological responses to overcome oxidative stress. In this study, oxidative damage, total antioxidant capacity and antioxidant enzymatic activities were analysed in functional and non-functional tomato autografts for eight days after grafting, considering scion and rootstock tissues separately. The results showed that oxidative damage, measured as lipid peroxidation, was controlled, especially in functional grafts. Scion tissues showed significant increases in total antioxidant capacity and activities of key antioxidant enzymes, including superoxide dismutase and catalase. Non-functional grafts showed elevated levels of class III peroxidase, potentially related to defensive suberisation and lignification. Principal component analysis revealed that antioxidant activities correlated dynamically with grafting stages, highlighting their critical role in stress mitigation. These results suggest that an efficient and asymmetric antioxidant response is essential for successful graft healing in tomato plants. Furthermore, different patterns in non-functional grafts underline the importance of redox balance in determining graft success.
  • Deepening the Role of Pectin in the Tissue Assembly Process During Tomato Grafting
    C. Frey, Susana Saez-Aguayo, A. Encina, J. Acebes
    Plants, 2024
    Cell walls play essential roles in cell recognition, tissue adhesion, and wound response. In particular, pectins as cell-adhesive agents are expected to play a key role in the early stages of grafting. To test this premise, this study focused on examining the dynamics of the accumulation and degree of methyl-esterification of pectic polysaccharides at the graft junctions using tomato autografts as an experimental model. Monosaccharide analysis showed a marked increase in homogalacturonan from 25% to 32 or 34% at the junction zones early after grafting. In addition, a decrease in the degree of homogalacturonan methyl-esterification up to 38% in the scion and 64% in the rootstock was observed in the first few days after grafting, accompanied by an increase in pectin methyl-esterase activity of up to 20–30% in the tissues surrounding the graft junction. These results shed light on the role of homogalacturonan in grafting and reinforce the key function of pectin as one of the most relevant cell wall components during the grafting process.
  • Phenolic compounds-enriched extract recovered from two-phase olive pomace serves as plant immunostimulants and broad-spectrum antimicrobials against phytopathogens including Xylella fastidiosa
    Marco Greco, María Fuertes-Rabanal, Carlos Frey, Carmine Del Grosso, Daniele Coculo, et al.
    Plant Stress, 2024
  • Immunohistochemical dynamics of cell wall matrix polymers during tomato autograft healing
    Carlos Frey, Nerea Martínez-Romera, Antonio Encina, José L. Acebes
    Plant Molecular Biology, 2023
    A large part of the production of tomato plants is grafted. Although it has recently been described that cell walls play an important role in tomato graft healing, the spatiotemporal dynamics of cell wall changes in this critical process remains largely unknown. The aim of this work was to immunolocalize changes in the major cell wall matrix components of autograft union tissues throughout the course of healing, from 1 to 20 days after grafting (DAG). Homogalacturonan was de novo synthetized and deposited in the cut edges, displaying the low methyl-esterified homogalacturonan a stronger labelling. Labelling of galactan side chains of rhamnogalacturonan increased until 8 DAG, although remarkably a set of cells at the graft union did not show labelling for this epitope. Changes in xylan immunolocalization were associated to the xylem vasculature development throughout, while those of xyloglucan revealed early synthesis at the cut edges. Arabinogalactan proteins increased up to 8 DAG and showed scion-rootstock asymmetry, with a higher extent in the scion. The combination of these changes appears to be related with the success of the autograft, specifically facilitating the adhesion phase between scion-rootstock tissues. This knowledge paves the way for improved grafting using methods that facilitate appropriate changes in the time and space dynamics of these cell wall compounds.
  • Non-invasive monitoring of tomato graft dynamics using thermography and fluorescence quantum yields measurements
    Carlos Frey, Andrés Hernández‐Barriuso, Antonio Encina, José Luis Acebes
    Physiologia Plantarum, 2023
    Grafting involves a sequence of modifications that may vary according to genotypes, grafting techniques and growing conditions. This process is often monitored using destructive methods, precluding the possibility of monitoring the entire process in the same grafted plant. The aim of this study was to test the effectiveness of two non-invasive methods -thermographic inference of transpiration and determination of chlorophyll quantum yields- for monitoring graft dynamics in tomato (Solanum lycopersicum L.) autografts, and to compare the results with other reliable measures: mechanical resistance parameters and xylem water potential. The mechanical resistance of grafted plants steadily increased from 6 days after grafting (DAG), 4.90±0.57 N/mm, to reach values similar to non-grafted plants at 16 DAG, 8.40±1.78 N/mm. Water potential showed an early decrease (from -0.34±0.16 MPa in non-grafted plants to -0.88±0.07 MPa at 2 DAG), recovering at 4 DAG to reach pre-grafting values at 12-16 DAG. Thermographic inference of transpiration dynamics displayed comparable changes. Monitoring maximum and effective quantum yield in functional grafts showed a comparable pattern: an initial decline, followed by recovery from 6 DAG onwards. Correlation analyses revealed a significant correlation between variation in temperature (thermographic monitoring of transpiration), water potential (r = 0.87; p = 0.02) and maximum tensile force (r = 0.75; p = 0.05). Additionally, we found a significant correlation between maximum quantum yield and some mechanical parameters. In conclusion, thermography monitoring, and to a lesser extent maximum quantum yield measurements, accurately depict changes in key parameters in grafted plants and serve as potential timing indicators of graft regeneration, rendering them valuable tools for monitoring graft functionality.
  • The graft framework: Quantitative changes in cell wall matrix polysaccharides throughout the tomato graft union formation
    Carlos Frey, Alba Manga-Robles, José Luis Acebes, Antonio Encina
    Carbohydrate Polymers, 2022
  • Histological description of Saxifraga paniculata leaves with special focus on structures that release CaCO3
    Santiago Michavila, Antonio Encina, Carlos Frey, Rafael Álvarez
    Plant Biosystems, 2022
  • Sequential extraction and analysis of cell wall polysaccharides from Inula viscosa leaves and stems
    Rayen Anouche, Aicha Bouhafsoun, Carlos Frey, José Luis Acebes
    Plant Biosystems, 2022
  • Tomato graft union failure is associated with alterations in tissue development and the onset of cell wall defense responses
    Carlos Frey, Rafael Álvarez, Antonio Encina, José Luis Acebes
    Agronomy, 2021
  • Histological changes associated with the graft union development in tomato
    Carlos Frey, José Luis Acebes, Antonio Encina, Rafael Álvarez
    Plants, 2020

RECENT SCHOLAR PUBLICATIONS

  • Biochemical diversity of macroalgal cell walls: Insights into the polysaccharide matrix
    C Frey, J Peláez, A Encina, H Mélida
    Algal Research, 104704 , 2026
    2026
  • Cell Wall Dynamics in Haustorial Development of Cuscuta campestris During Parasitism on Differentially Susceptible Hosts
    C Frey, L López-López, A Martínez-Toral, D Castro, JL Acebes
    International Journal of Molecular Sciences 27 (4), 1914 , 2026
    2026
  • The role of plant cell walls in pest resistance: current insights and future perspectives
    MM Perez-Alonso, L Talavera-Mateo, D Ojeda-Martinez, ...
    Journal of Experimental Botany 76 (20), 5775-5790 , 2025
    2025
    Citations: 2
  • Photosynthesis and stress tolerance: cell walls at the cross-roads
    MJ Clemente-Moreno, C Frey, L López-Serrano, JL Acebes, J Flexas, ...
    Journal of Experimental Botany 76 (17), 4884-4895 , 2025
    2025
    Citations: 6
  • Harnessing macroalgal cell walls to trigger immunity in Arabidopsis thaliana
    J Peláez, C Frey, D Rebaque, F Vilaplana, A Encina, H Mélida
    Plant Stress 15, 100783 , 2025
    2025
    Citations: 2
  • Deciphering Antioxidant Responses in Tomato Autografts
    C Frey, A Hernández-Barriuso, JL Acebes, A Encina
    Antioxidants 14 (2), 234 , 2025
    2025
    Citations: 2
  • Deepening the role of pectin in the tissue assembly process during tomato grafting
    C Frey, S Saez-Aguayo, A Encina, JL Acebes
    Plants 13 (24), 3519 , 2024
    2024
    Citations: 2
  • Phenolic compounds-enriched extract recovered from two-phase olive pomace serves as plant immunostimulants and broad-spectrum antimicrobials against phytopathogens including …
    M Greco, M Fuertes-Rabanal, C Frey, C Del Grosso, D Coculo, P Moretti, ...
    Plant Stress 14, 100655 , 2024
    2024
    Citations: 19
  • Immunohistochemical dynamics of cell wall matrix polymers during tomato autograft healing
    C Frey, N Martínez-Romera, A Encina, JL Acebes
    Plant Molecular Biology 113 (6), 353-365 , 2023
    2023
    Citations: 14
  • Una iniciativa de gamificación para el aprendizaje de la biología de las plantas basada en un juego de cartas
    C Frey, A Manga-Robles, I del Hierro, A Encina, ML Centeno, ...
    Boletín de la Sociedad Española de Biología de las Plantas 73, 36-40 , 2023
    2023
    Citations: 1
  • Non‐invasive monitoring of tomato graft dynamics using thermography and fluorescence quantum yields measurements
    C Frey, A Hernández‐Barriuso, A Encina, JL Acebes
    Physiologia Plantarum 175 (3), e13935 , 2023
    2023
    Citations: 6
  • Planta: un proyecto de aprendizaje basado en juegos en Fisiología Vegetal
    C Frey, A Manga-Robles, I del Hierro, A Encina, ML Centeno, ...
    VI Jornadas de Innovación Docente de la Universidad de León. León, 10-11 , 2023
    2023
    Citations: 2
  • Immunohistochemical dynamics of cell wall matrix polymers during tomato autograft healing
    C Frey Domínguez, N Martínez Romera, AE Encina García, ...
    Plant Molecular Biology , 2023
    2023
  • Experiencias fascinantes en la docencia de la Biología de las Plantas
    JL Acebes, ML Centeno Martín, A Encina, C Frey, P García Angulo, ...
    AmbioCiencias: revista de divulgación 21, 161-174 , 2023
    2023
  • Exploring the physiological, histological and cell wall modifications throughout the grafting of tomato (Solanum lycopersicum L.) plants
    C Frey Domínguez
    Exploring the physiological, histological and cell wall modifications … , 2023
    2023
  • Sequential extraction and analysis of cell wall polysaccharides from Inula viscosa leaves and stems
    R Anouche, A Bouhafsoun, C Frey, JL Acebes
    Plant Biosystems-An International Journal Dealing with all Aspects of Plant … , 2022
    2022
  • Histological description of Saxifraga paniculata leaves with special focus on structures that release CaCO 3
    S Michavila, A Encina, C Frey, R Álvarez
    Plant Biosystems-An International Journal Dealing with all Aspects of Plant … , 2022
    2022
    Citations: 4
  • The graft framework: Quantitative changes in cell wall matrix polysaccharides throughout the tomato graft union formation
    C Frey, A Manga-Robles, JL Acebes, A Encina
    Carbohydrate polymers 276, 118781 , 2022
    2022
    Citations: 21
  • Tomato graft union failure is associated with alterations in tissue development and the onset of cell wall defense responses
    C Frey, R Álvarez, A Encina, JL Acebes
    Agronomy 11 (6), 1197 , 2021
    2021
    Citations: 26
  • Tomato Graft Union Failure Is Associated with Alterations in Tissue Development and the Onset of Cell Wall Defense Responses. Agronomy 2021, 11, 1197
    C Frey, R Álvarez, A Encina, JL Acebes
    s Note: MDPI stays neutral with regard to jurisdictional claims in published … , 2021
    2021

MOST CITED SCHOLAR PUBLICATIONS

  • Tomato graft union failure is associated with alterations in tissue development and the onset of cell wall defense responses
    C Frey, R Álvarez, A Encina, JL Acebes
    Agronomy 11 (6), 1197 , 2021
    2021
    Citations: 26
  • The graft framework: Quantitative changes in cell wall matrix polysaccharides throughout the tomato graft union formation
    C Frey, A Manga-Robles, JL Acebes, A Encina
    Carbohydrate polymers 276, 118781 , 2022
    2022
    Citations: 21
  • Histological changes associated with the graft union development in tomato
    C Frey, JL Acebes, A Encina, R Álvarez
    Plants 9 (11), 1479 , 2020
    2020
    Citations: 20
  • Phenolic compounds-enriched extract recovered from two-phase olive pomace serves as plant immunostimulants and broad-spectrum antimicrobials against phytopathogens including …
    M Greco, M Fuertes-Rabanal, C Frey, C Del Grosso, D Coculo, P Moretti, ...
    Plant Stress 14, 100655 , 2024
    2024
    Citations: 19
  • Immunohistochemical dynamics of cell wall matrix polymers during tomato autograft healing
    C Frey, N Martínez-Romera, A Encina, JL Acebes
    Plant Molecular Biology 113 (6), 353-365 , 2023
    2023
    Citations: 14
  • Photosynthesis and stress tolerance: cell walls at the cross-roads
    MJ Clemente-Moreno, C Frey, L López-Serrano, JL Acebes, J Flexas, ...
    Journal of Experimental Botany 76 (17), 4884-4895 , 2025
    2025
    Citations: 6
  • Non‐invasive monitoring of tomato graft dynamics using thermography and fluorescence quantum yields measurements
    C Frey, A Hernández‐Barriuso, A Encina, JL Acebes
    Physiologia Plantarum 175 (3), e13935 , 2023
    2023
    Citations: 6
  • Histological description of Saxifraga paniculata leaves with special focus on structures that release CaCO 3
    S Michavila, A Encina, C Frey, R Álvarez
    Plant Biosystems-An International Journal Dealing with all Aspects of Plant … , 2022
    2022
    Citations: 4
  • The role of plant cell walls in pest resistance: current insights and future perspectives
    MM Perez-Alonso, L Talavera-Mateo, D Ojeda-Martinez, ...
    Journal of Experimental Botany 76 (20), 5775-5790 , 2025
    2025
    Citations: 2
  • Harnessing macroalgal cell walls to trigger immunity in Arabidopsis thaliana
    J Peláez, C Frey, D Rebaque, F Vilaplana, A Encina, H Mélida
    Plant Stress 15, 100783 , 2025
    2025
    Citations: 2
  • Deciphering Antioxidant Responses in Tomato Autografts
    C Frey, A Hernández-Barriuso, JL Acebes, A Encina
    Antioxidants 14 (2), 234 , 2025
    2025
    Citations: 2
  • Deepening the role of pectin in the tissue assembly process during tomato grafting
    C Frey, S Saez-Aguayo, A Encina, JL Acebes
    Plants 13 (24), 3519 , 2024
    2024
    Citations: 2
  • Planta: un proyecto de aprendizaje basado en juegos en Fisiología Vegetal
    C Frey, A Manga-Robles, I del Hierro, A Encina, ML Centeno, ...
    VI Jornadas de Innovación Docente de la Universidad de León. León, 10-11 , 2023
    2023
    Citations: 2
  • Una iniciativa de gamificación para el aprendizaje de la biología de las plantas basada en un juego de cartas
    C Frey, A Manga-Robles, I del Hierro, A Encina, ML Centeno, ...
    Boletín de la Sociedad Española de Biología de las Plantas 73, 36-40 , 2023
    2023
    Citations: 1
  • El Bierzo: la joya del noroeste
    C Frey, J González, S Vizcay
    Ambiens Ibericus–Revista de divulgación medioambiental 1, 24-34 , 2020
    2020
    Citations: 1
  • Evolución de la distribución de las pectinas en la zona de unión en injertos de tomate
    N Martínez Romera, C Frey, JL Acebes
    AmbioCiencias: revista de divulgación 18, 41-56 , 2020
    2020
    Citations: 1
  • Biochemical diversity of macroalgal cell walls: Insights into the polysaccharide matrix
    C Frey, J Peláez, A Encina, H Mélida
    Algal Research, 104704 , 2026
    2026
  • Cell Wall Dynamics in Haustorial Development of Cuscuta campestris During Parasitism on Differentially Susceptible Hosts
    C Frey, L López-López, A Martínez-Toral, D Castro, JL Acebes
    International Journal of Molecular Sciences 27 (4), 1914 , 2026
    2026
  • Immunohistochemical dynamics of cell wall matrix polymers during tomato autograft healing
    C Frey Domínguez, N Martínez Romera, AE Encina García, ...
    Plant Molecular Biology , 2023
    2023
  • Experiencias fascinantes en la docencia de la Biología de las Plantas
    JL Acebes, ML Centeno Martín, A Encina, C Frey, P García Angulo, ...
    AmbioCiencias: revista de divulgación 21, 161-174 , 2023
    2023