DISSECTING PLANT DEFENCE-GROWTH TRADE-OFFS ESTABLISHED UPON PLANT-PEST INTERACTIONS


Group leader: Estrella Santamaría Fernández - Assistant Professor
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Personnel:

 

Orcid: 0000-0003-4999-6227
Scopus: 24336181000
ResearchID: 1186299


Overview:


“Our main goal is to decipher the molecular mechanisms behind the defence-growth trade-off stablished in plants upon pest infestation. A comprehensive understanding of this trade-off and the strategies proposed to tackle it would be very helpful in the design of pest management strategies increasing plant resistance and minimizing or abolishing the penalty in plant growth/reproduction”.


Research lines:

1. The price of the plant induced defences


Plants have evolved constitutive and inducible defences in response to phytophagous pests. As a result, herbivores react to plant defences by developing multiple strategies to suppress them, and plants counterattack by implementing more emergency responses. Constitutive or permanent defences are constantly activated but they are not always needed, entailing high cost for the plants. In this sense, the plant defence theory suggests that inducible resistance has evolved to reduce the cost of constitutive defences in the absence of enemies, nevertheless inducible defence still incurs costs. We are interested in deciphering the price of these induced defences and the molecular mechanisms behind them. In a recent meta-analysis, we showed that the activation of plant defences in response to phytophagous infestation has a penalty in plant growth, photosynthesis and/or reproduction, being the variables surrounding plant-pest interaction (plant ontogenetic stage, plant host, pest feeding guild, infestation magnitude and length) of crucial importance in the final trade-off (Garcia et al., 2021).


FIGURE 1 | Effect sizes on general parameters related to fitness. Garcia et al., 2021.


FIGURE 2 | A diagram depicting the concept of growth-defense trade-offs, the parameters to evaluate the fitness and the main variables involved. Garcia et al., 2021.

 


2. The molecular mechanism behind the defence-growth trade-off stablished in Arabidopsis upon spider mite infestation


In this project the trade-off stablished in Arabidopsis thaliana upon Tetranychus urticae (spider mite) infestation is studied. These two organisms are model species in the study of plant-pest interphase, being the spider mite one of the major pests in agriculture. The integration of fitness measurements with transcriptomic and metabolomic results will enable us to draw a molecular landscape of the underlying mechanisms involved in this trade-off.


FIGURE 3 | Evaluation of the defense-growth trade-off established upon A. thaliana - T. urticae. The data integration of fitness parameters with transcriptomic and metabolomic results will enable us to achieve a better understanding of the defense-growth tradeoff.

 


3. Priming as a mechanism to mitigate the defence-growth trade-off stablished in plants upon pest infestation


Plants have developed the capacity to respond to previous stimuli by enhancing the activation of inducible defences upon later infestation or herbivore attack. This physiological process, known as defence priming, triggers a minor part of the plant defence response and enables prompter or more effective reactions against future biotic or abiotic stresses. However, although primed plants theoretically endure fewer costs in relation to the direct activation of defences, the physiological alterations produced while shifting the plant to the alert are bound to cause some resource allocation and/or ecological costs. Under this scenario, our objective is to identify priming agents that produce higher resistance, minimizing the penalty in plant fitness and to unveil the molecular basis of how these priming treatments modulate the defence-growth trade-off established upon the infestation. Besides our Arabidopsis-T. urticae working model, we will extend our analyses to the related crop Brassica rapa and the herbivorous insect Pieris brassicae. This will most likely pave the way for more sustainable crop protection practices without penalization on plant fitness.


FIGURE 4 | Simplified scheme of the potential effect of “priming” over the plant defence-growth trade-off.

 

Funding:

Estudio del papel de las hormonas de crecimiento de plantas en el compromiso defensa- crecimiento establecido en la interacción planta-plaga «Ayudas para Incentivar la Consolidación Investigadora 2022». Proyecto CNS2022-135194 financiado por MCIN/AEI /10.13039/501100011033 y por la Unión Europea NextGenerationEU/PRTR

 


Understanding how important pest and viral diseases will evolve in the context of climate change. EoI-MCBGP21: PLANTADAPT_02_CLIMATEPLANT-PEST-VIRUSINTERACT. Programa Severo Ochoa Ayuda CEX2020-000999-S financiada por MCIN/AEI /10.13039/501100011033.

          


Plant-pest interaction. Ayudas para contratos Ramón y Cajal. Ayuda RYC-2017-21814 financiada por MCIN/AEI /10.13039/501100011033 y FSE “El FSE invierte en tu futuro”.


Compromiso defensa-crecimiento en Arabidopsis en respuesta a la infestación con T. urticae. Acción financiada por la Comunidad de Madrid en el marco del Convenio Plurianual con la Universidad Politécnica de Madrid en la línea de actuación estímulo a la investigación de jóvenes doctores (APOYO-JOVENES-SUR6Q9-22-YTFC3Z).

 


Effect of seed defence priming on plant defence-growth trade-off established upon plant-pest interaction. Proyectos I+D+i -Modalidades «Retos Investigación» y «Generación de Conocimiento». Proyecto PID2020-112756RA-I00 financiado por MCIN/ AEI /10.13039/501100011033.


 

 


Representative Publications

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


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


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


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


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


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


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


Santamaria, M.E., Garcia, A., Arnaiz, A., Rosa-Diaz, I., Romero-Hernandez, G., Diaz, I., Martinez, M. 2021. Comparative transcriptomics reveals hidden issues in the plant response to arthropod herbivores. Journal of Integrative Plant Biology 63, 312–326. 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


Santamaría, M.E., Martínez, M., Arnaiz, A., Rioja, C., Burow, M., Grbic, V., Díaz, I. 2019. An Arabidopsis TIR-Lectin Two-Domain Protein Confers Defense Properties against Tetranychus urticae. Plant Physiology 179, 1298–1314. DOI: 10.1104/pp.18.00951


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


Arnaiz, A., Talavera-Mateo, L., Gonzalez-Melendi, P., Martinez, M., Diaz, I., Santamaria, M.E. 2018. Arabidopsis Kunitz Trypsin Inhibitors in Defense Against Spider Mites. Frontiers in Plant Science 9, 986. DOI: 10.3389/fpls.2018.00986


Santamaría, M.E., Arnaiz, A., Velasco-Arroyo, B., Grbic, V., Diaz, I., Martinez, M. 2018. Arabidopsis response to the spider mite Tetranychus urticae depends on the regulation of reactive oxygen species homeostasis. Scientific Reports 8, 9432. DOI: 10.1038/s41598-018-27904-1


Santamaría, M.E., Auger, P., Martínez, M., Migeon, A., Castañera, P., Díaz, I., Navajas, M., Ortego, F. 2018. Host plant use by two distinct lineages of the tomato red spider mite, Tetranychus evansi, differing in their distribution range. Journal of Pest Science 91, 169–179. DOI: 10.1007/s10340-017-0852-1


Santamaría, M.E., Martinez, M., Arnaiz, A., Ortego, F., Grbic, V., Diaz, I. 2017. MATI, a Novel Protein Involved in the Regulation of Herbivore-Associated Signaling Pathways. Frontiers in Plant Science 8, 975. DOI: 10.3389/fpls.2017.00975


Zhurov, V., Navarro, M., Bruinsma, K.A., Arbona, V., Santamaria, M.E., Cazaux, M., Wybouw, N., Osborne, E.J., Ens, C., Rioja, C., Vermeirssen, V., Rubio-Somoza, I., Krishna, P., Diaz, I., Schmid, M., Gómez-Cadenas, A., Van de Peer, Y., Grbić, M., Clark, R.M., Van Leeuwen, T., Grbić, V. 2014. Reciprocal Responses in the Interaction between Arabidopsis and the Cell-Content-Feeding Chelicerate Herbivore Spider Mite. Plant Physiology 164, 384–399. DOI: 10.1104/pp.113.231555