MOLECULAR PLANT-PEST INTERACTIONS

The control of pests that attack our crops is one of the major challenges and costs in agriculture today. It is predicted that the importance of arthropod pests will increase as a result of global warming and that new problems will arise from the emergence of novel pests into agroecosystems. In this context, the main objective of our group is to decipher how plants recognize and respond to a particular herbivore attack, how climate change affects these interactions, and how defences are fine-tune regulated to limit costs of resistance. To identify genes, proteins and molecules with potential use to control pests as an alternative to non-natural compounds, is an additional goal.

Our current plant-pest model is formed by the plant Arabidopsis thaliana and the phytophagous arthropod Tetranychus urticae. In addition, we include in our research crop species as bean and brassicas as hosts. The two-spotted spider mite T. urticae is a cosmopolitan agricultural acarian, considered one of the most significant agricultural threats since it has a short life cycle, high offspring production and an extraordinary ability to develop pesticide resistance. It feeds on over 1,100 documented host plants, 150 of them of agricultural importance. Spider mites pierce individual mesophyll parenchymatic cells using stylets to suck their nutrients without damaging epidermal cells. They produce severe chlorosis and the consequent reduction in crop yield.

Tetranychus uticae feeding on bean

Although, mites are our main interest, we have expanded our scope to other arthropod herbivores including two chewing lepidopteran species at larval stages, Pieris brassicae and Spodoptera exigua, to understand whether the feeding mode modify, not only plant responses but also the regulatory mechanisms involved in modulating these responses.

Along the last years, we have focused our attention in deciphering how plants respond to spider mite infestation, analysing since the earliest step involved in the mite recognition mediated by plant receptors which prompt a transduction pathway, until the final generation of defences. We have identified and characterized receptors at cell surface, intracellular receptors, regulators, and defensive compounds participating either in primary immune system machinery (Pattern-Triggered Immunity, PTI) and/or in secondary robust defence responses (Effector-Triggered Immunity, ETI). A good number of genes/proteins/metabolites with defence function and related pathways, have been described. The role of hormones, mainly JA, JA-derivatives and SA have resulted crucial modulators of defences.

                   Scheme of plant responses to spider mite feeding                                      Molecular network of expressed genes upon 30 min mite infestation   

All these data have pushed us to deepen in two novel research lines developed in more recent years. First, we have focused on the analysis of the regulatory role of hormones, mainly JA and JA-catabolism in defence to mites. Concomitantly, we have tried to clarify the relation between ABA and stomata aperture in the plant-mite scenario, since trichomes act as entry sites where piercing-sucking mites insert their stylets to access nutrient cells. The second research line has been to study the fine-tune regulatory mechanisms of plant defences induction, mediated by microRNAS. In particular, to understand how the miRNA825-5p controls the production of several Leucine Rich Repeat receptors with a TIR domain (TNLs) at the post-transcriptional level, and their role to limit costs of plant resistance to herbivores.

Additionally, the characterization of novel defensive molecules linked to cyanogenesis, such is the hydroxynitrile lyase (HNL), prompted us to prepare a proposal and to apply for a Proof of Concept project. The initial idea was to transfer basic knowledge generated in model plants to crops, to be applied for pest control. Thus, we are studying the differential response of cyanogenic and non-cyanogenic plants, Phaseolus lunatus and Phaseolus vulgaris, respectively, to spider mite infestation. The final goal is to produce novel recombinant proteins from plant origin with defence properties to control phytophagous mites and insects.

Since it is predicted that the importance of pests will increase as a result of global warming and that new pest problems will arise from the introduction of invasive species into agroecosystems as well as emergence of novel pests that had minor significance previously. Temperature and water availability associated with climate change have profound effects on the plant-herbivore interactions. To dissect these intricate interactions, we are using novel technologies to understand how the gene expression changes as a function of climate change parameters and how these changes are linked to fitness outputs for these organisms. In this context, our main goal has been to know how the molecular signalling is modified upon a particular herbivore attack and how climate change affects these interactions. The Arabidopsis/T. urticae pair is a good starting model because of under increased temperatures and drought stress associated with climate change, Tetranychidae species shorten their life cycle, produce more generations per year and appears earlier in the season and on a wider range of hosts. To a better understanding of the molecular pathways, we pretend to extend our analyses to a second herbivore, the insect P. brassicae, and to crop plant Brassica rapa. Overall, the obtained knowledge will permit to dissect the molecular effects of climate factors on the plant/herbivore interactions and to develop new tools for an efficient and environmentally-friendly pest management under conditions of changing climate.

Experimental design to decipher the effect of increased temperatures on plant-pest interactions

Funding

• EFECTO DE LAS CONDICIONES AMBIENTALES SOBRE LAS REDES MOLECULARES QUE CONECTAN PERCEPCIÓN Y RESPUESTAS DE LA PLANTA A PLAGAS DE ARTRÓPODOS - CLIMOLPEST. Ministerio de Ciencia e Innovación. Proyectos I+D+i - Modalidades “Retos Investigación” y “Generación de Conocimiento”. Proyecto PID2020-115219RB-I00 financiado por MCIN/ AEI /10.13039/501100011033.
  
  

• DE ESPECIES MODELO A CULTIVOS: COMPUESTOS DERIVADOS DE CIANOHIDRINAS EN LA PROTECCIÓN DE CULTIVOS CONTRA PLAGAS - CYHY-CP. Ministerio de Ciencia e Innovación. Proyectos de I+D+ i "Pruebas de concepto". Proyecto PDC2021-121055-I00 financiado por MCIN/AEI /10.13039/501100011033 y por la Unión Europea Next GenerationEU/ PRTR.
  
  

• APRENDIENDO DE LA NATURALEZA: INTERACCIONES MULTITRÓFICAS PARA LA PROTECCIÓN DE CULTIVOS Y BOSQUES. Ministerio de Ciencia e Innovación. Acciones de Dinamización «Redes de Investigación». Ayuda RED2018-102407-T financiada por MCIN/ AEI /10.13039/501100011033.
  
  

• SEÑALIZACIÓN REDOX Y REGULACIÓN POST-TRADUCCIONAL EN EL DESARROLLO Y RESPUESTA A ESTRÉS DE LAS PLANTAS. Ministerio de Ciencia e Innovación. Acciones de Dinamización «Redes de Investigación». Ayuda RED2018-102397-T financiada por MCIN/ AEI /10.13039/501100011033.
  
  

Representative Publications

Perez-Alonso, M.M., Talavera-Mateo, L., Ojeda-Martinez, D., Barcenilla-Valcárcel, L., Montesinos, Á., Garcia, A., Frey, C., Boter, M., Martinez, M., Diaz, I., Santamaria, M.E. 2025. The role of plant cell walls in pest resistance: current insights and future perspectives. Journal of Experimental Botany eraf306. DOI: 10.1093/jxb/eraf306

Rosa-Diaz, I., Lopez-Marquez, D., Beuzon, C.R., Diaz, I. 2025. miR825-5p-regulated TNLs govern Arabidopsis resistance to Tetranychus urticae and Pieris brassicae. New Phytologist. DOI: 10.1111/nph.70411

Contreras, E., Martinez, M. 2025. Warm temperature and mild drought remodel transcriptome and alter Arabidopsis responses to mite herbivory. Physiologia Plantarum 177, e70219. DOI: 10.1111/ppl.70219

Ojeda-Martinez, D., Diaz, I., Santamaria, M.E., Ortego, F. 2024. Comparative genomics reveals carbohydrate enzymatic fluctuations and herbivorous adaptations in arthropods. Computational and Structural Biotechnology Journal 23, 3744–3758. DOI: 10.1016/j.csbj.2024.10.027

Garcia, A., Talavera-Mateo, L., Petrik, I., Oklestkova, J., Novak, O., Santamaria, M.E. 2024. Spider mite infestation triggers coordinated hormonal trade-offs enabling plant survival with a fitness cost. Physiologia Plantarum 176, e14479. DOI: 10.1111/ppl.14479

Boter, M., Diaz, I. 2024. Contrasting defence mechanisms against spider mite infestation in cyanogenic and non-cyanogenic legumes. Plant Science 345, 112118. DOI: 10.1016/j.plantsci.2024.112118

Rosa-Díaz, I., Rowe, J., Cayuela-Lopez, A., Arbona, V., Díaz, I., Jones, A.M. 2024. Spider mite herbivory induces an abscisic acid-driven stomatal defense. Plant Physiology kiae215. DOI: 10.1093/plphys/kiae215

Martinez, M., Diaz, I. 2024. Plant Cyanogenic-Derived Metabolites and Herbivore Counter-Defences. Plants 13, 1239. DOI: 10.3390/plants13091239

Contreras, E., Martinez, M. 2024. The RIN4-like/NOI proteins NOI10 and NOI11 modulate the response to biotic stresses mediated by RIN4 in Arabidopsis. Plant Cell Reports 43, 70. DOI: 10.1007/s00299-024-03151-9

Montesinos, Á., Sacristán, S., del Prado-Polonio, P., Arnaiz, A., Díaz-González, S., Diaz, I., Santamaria, M.E. 2024. Contrasting plant transcriptome responses between a pierce-sucking and a chewing herbivore go beyond the infestation site. BMC Plant Biology 24, 120. DOI: 10.1186/s12870-024-04806-1

Arnaiz, A., Romero-Puertas, M.C., Santamaria, M.E., Rosa-Diaz, I., Arbona, V., Muñoz, A., Grbic, V., González-Melendi, P., Mar Castellano, M., Sandalio, L.M., Martinez, M., Diaz, I. 2023. The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae. Redox Biology 67, 102902. DOI: 10.1016/j.redox.2023.102902

Bruinsma, K., Rioja, C., Zhurov, V., Santamaria, M.E., Arbona, V., Navarro, M., Cazaux, M., Auger, P., Migeon, A., Wybouw, N., Van Leeuwen, T., Diaz, I., Gómez-Cadenas, A., Grbic, M., Navajas, M., Grbic, V. 2023. Host-adaptation and specialization in Tetranychidae mites. Plant Physiology kiad412. DOI: 10.1093/plphys/kiad412

Arnaiz, A., Lucas Vallejo-García, J., Vallejos, S., Diaz, I. 2023. Isolation and Quantification of Mandelonitrile from Arabidopsis thaliana Using Gas Chromatography/Mass Spectrometry. Bio-protocol 13. DOI: 10.21769/BioProtoc.4700

Talavera-Mateo, L., Garcia, A., Santamaria, M.E. 2023. A comprehensive meta-analysis reveals the key variables and scope of seed defense priming. Frontiers in Plant Science 14. DOI: 10.3389/fpls.2023.1208449

Rosa-Diaz, I., Santamaria, M.E., Acien, J.M., Diaz, I. 2023. Jasmonic acid catabolism in Arabidopsis defence against mites. Plant Science 334, 111784. DOI: 10.1016/j.plantsci.2023.111784

Boter, M., Diaz, I. 2023. Cyanogenesis, a Plant Defence Strategy against Herbivores. International Journal of Molecular Sciences 24, 6982. DOI: 10.3390/ijms24086982

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

Romero-Hernandez, G., Martinez, M. 2022. Opposite roles of MAPKKK17 and MAPKKK21 against Tetranychus urticae in Arabidopsis. Frontiers in Plant Science 13. DOI: 10.3389/fpls.2022.1038866

Contreras, E., Martinez, M. 2022. Comparative and evolutionary analysis of Arabidopsis RIN4-like/NOI proteins induced by herbivory. PLOS ONE 17, e0270791. DOI: 10.1371/journal.pone.0270791

Garcia, A., Talavera-Mateo, L., Santamaria, M.E. 2022. An automatic method to quantify trichomes in Arabidopsis thaliana. Plant Science 323, 111391. DOI: 10.1016/j.plantsci.2022.111391

Arnaiz, A., Santamaria, M.E., Rosa-Diaz, I., Garcia, I., Dixit, S., Vallejos, S., Gotor, C., Martinez, M., Grbic, V., Diaz, I. 2022. Hydroxynitrile lyase defends Arabidopsis against Tetranychus urticae. Plant Physiology kiac170. DOI: 10.1093/plphys/kiac170

Suzuki, T., Broufas, G., Smagghe, G., Ortego, F., Broekgaarden, C., Diaz, I. 2021. Editorial: Plant-Pest Interactions Volume III: Coleoptera and Lepidoptera. Frontiers in Plant Science 12, 1674. DOI: 10.3389/fpls.2021.730290

Ortego, F., Broekgaarden, C., Suzuki, T., Broufas, G., Smagghe, G., Diaz, I. 2021. Editorial: Plant-Pest Interactions Volume II: Hemiptera. Frontiers in Plant Science 12, 1978. DOI: 10.3389/fpls.2021.748999

Broufas, G., Ortego, F., Suzuki, T., Smagghe, G., Broekgaarden, C., Diaz, I. 2022. Editorial: Plant-Pest Interactions Volume I: Acari and Thrips. Frontiers in Plant Science 12. DOI: 10.3389/fpls.2021.773439

Ojeda-Martinez, D., Diaz, I., Santamaria, M.E. 2022. Transcriptomic Landscape of Herbivore Oviposition in Arabidopsis: A Systematic Review. Frontiers in Plant Science. DOI: 10.3389/fpls.2021.772492

Pérez-Alonso, M.-M., Sánchez-Parra, B., Ortiz-García, P., Santamaría, M.E., Díaz, I., Pollmann, S. 2021. Jasmonic Acid-Dependent MYC Transcription Factors Bind to a Tandem G-Box Motif in the YUCCA8 and YUCCA9 Promoters to Regulate Biotic Stress Responses. International Journal of Molecular Sciences 22, 9768. DOI: 10.3390/ijms22189768

Muñoz, A., Santamaria, M.E., Fernández-Bautista, N., Mangano, S., Toribio, R., Martínez, M., Berrocal-Lobo, M., Díaz, I., Castellano, M.M. 2021. The co-chaperone HOP3 participates in jasmonic acid signaling by regulating CORONATINE INSENSITIVE 1 activity. Plant Physiology. DOI: 10.1093/plphys/kiab334

Ojeda-Martinez, D., Martinez, M., Diaz, I., Estrella Santamaria, M. 2021. Spider mite egg extract modifies Arabidopsis response to future infestations. Scientific Reports 11, 17692. DOI: 10.1038/s41598-021-97245-z

Gandullo, J., Álvarez, R., Feria, A.-B., Monreal, J.-A., Díaz, I., Vidal, J., Echevarría, C. 2021. A conserved C-terminal peptide of sorghum phosphoenolpyruvate carboxylase promotes its proteolysis, which is prevented by Glc-6P or the phosphorylation state of the enzyme. Planta 254, 43. DOI: 10.1007/s00425-021-03692-3

Garcia, A., Santamaria, M.E., Diaz, I., Martinez, M. 2021. Disentangling transcriptional responses in plant defense against arthropod herbivores. Scientific Reports 11, 12996. DOI: 10.1038/s41598-021-92468-6

Gomez-Sanchez, A., Santamaria, M.E., Gonzalez-Melendi, P., Muszynska, A., Matthess, C., Martinez, M., Diaz, I. 2021. Repression of barley cathepsins, HvPap-19 and HvPap-1, differentially alters grain composition and delays germination. Journal of Experimental Botany. DOI: 10.1093/jxb/erab007

Garcia, A., Martinez, M., Diaz, I., Santamaria, M.E. 2021. The Price of the Induced Defense Against Pests: A Meta-Analysis. Frontiers in Plant Science 11, 2285. DOI: 10.3389/fpls.2020.615122

Arnaiz, A., Rosa-Diaz, I., Romero-Puertas, M.C., Sandalio, L.M., Diaz, I. 2021. Nitric Oxide, an Essential Intermediate in the Plant-Herbivore Interaction. Frontiers in Plant Science 11, 2029. DOI: 10.3389/fpls.2020.620086

Santamaria, ME., Garcia, A., Arnaiz, A., Rosa-Diaz, I ., Romero-Hernandez, G., Diaz, I., Martinez, M. 2020. Comparative transcriptomics reveals hidden issues in the plant response to arthropod herbivores. Journal of Integrative Plant Biology. DOI: 10.1111/jipb.13026

Ojeda-Martinez, D., Martinez, M., Diaz, I., Santamaria, M.E. 2020. Saving time maintaining reliability: a new method for quantification of Tetranychus urticae damage in Arabidopsis whole rosettes. BMC Plant Biology 20, 397. DOI: 10.1186/s12870-020-02584-0

Santamaria, M.E., Arnaiz, A., Rosa-Diaz, I., González-Melendi, P., Romero-Hernandez, G., Ojeda-Martinez, D.A., Garcia, A., Contreras, E., Martinez, M., Diaz, I. 2020. Plant Defenses Against Tetranychus urticae: Mind the Gaps. Plants 9, 464. DOI: 10.3390/plants9040464

Martinez, M. 2019. Editorial for Special Issue “Molecular Advances in Wheat and Barley”. International Journal of Molecular Sciences 20, 3501. DOI: 10.3390/ijms20143501

Rubio, M.C., Calvo‐Begueria, L., Díaz‐Mendoza, M., Elhiti, M., Moore, M., Matamoros, M.A., James, E.K., Díaz, I., Pérez‐Rontomé, C., Villar, I., Sein‐Echaluce, V.C., Hebelstrup, K.H., Dietz, K.-J., Becana, M. 2019. Phytoglobins in the nuclei, cytoplasm and chloroplasts modulate nitric oxide signaling and interact with abscisic acid. The Plant Journal. DOI: 10.1111/tpj.14422

Arnaiz, A., Martinez, M., Gonzalez-Melendi, P., Grbic, V., Diaz, I., Santamaria, M.E. 2019. Plant Defenses Against Pests Driven by a Bidirectional Promoter. Frontiers in Plant Science 10, 930. DOI: 10.3389/fpls.2019.00930

Sperotto, R.A., Grbic, V., Pappas, M.L., Leiss, K.A., Kant, M.R., Wilson, C.R., Santamaria, M.E., Gao, Y. 2019. Editorial: Plant Responses to Phytophagous Mites/Thrips and Search for Resistance. Frontiers in Plant Science 10, 866. DOI: 10.3389/fpls.2019.00866

Calero‐Muñoz, N., Exposito‐Rodriguez, M., Collado‐Arenal, A.M., Rodríguez-Serrano, M., Laureano‐Marín, A.M., Santamaría, M.E., Gotor, C., Díaz, I., Mullineaux, P.M., Romero‐Puertas, M.C., Olmedilla, A., Sandalio, L.M. 2019. Cadmium induces ROS-dependent pexophagy in Arabidopsis leaves. Plant, Cell & Environment. DOI: 10.1111/pce.13597

Martinez, M., Gómez-Cabellos, S., Giménez, M.J., Barro, F., Diaz, I., Diaz-Mendoza, M. 2019. Plant Proteases: From Key Enzymes in Germination to Allies for Fighting Human Gluten-Related Disorders. Frontiers in Plant Science 10, 721. DOI: 10.3389/fpls.2019.00721

Diaz-Mendoza, M., Diaz, I., Martinez, M. 2019. Insights on the Proteases Involved in Barley and Wheat Grain Germination. International Journal of Molecular Sciences 20, 2087. DOI: 10.3390/ijms20092087

Gandullo, J., Monreal, J.-A., Álvarez, R., Díaz, I., García-Mauriño, S., Echevarría, C. 2019. Anionic Phospholipids Induce Conformational Changes in Phosphoenolpyruvate Carboxylase to Increase Sensitivity to Cathepsin Proteases. Frontiers in Plant Science 10. DOI: 10.3389/fpls.2019.00582

Santamaria, M.E., Martinez, M., Arnaiz, A., Rioja, C., Burow, M., Grbic, V., Diaz, I. 2019. An Arabidopsis TIR-lectin two-domain protein confers defence properties against Tetranychus urticae. Plant Physiology pp.00951.2018. DOI: 10.1104/pp.18.00951

Spider mite damage quantification method

Ojeda et al., 2022 Network Analysis