MOLECULAR PLANT-PEST INTERACTIONS

Group leader: Isabel Díaz Rodríguez - Professor

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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 and how climate change affects these interactions. To identify genes, proteins and molecules with potential use to control pests is an additional goal.

1. Deciphering plant defence responses to pest infestations.

Our current plant-pest model is formed by the plant Arabidopsis thaliana and the phytophagous arthropod Tetranychus urticae. In addition, crop species as tomato, bean and brassicas are also host pest targets used in our research. 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. Our research tries to decode the plant defence responses (genes, signalling pathways, molecules and hormonal regulation) that confer resistance to mites and to apply the knowledge gained through basic science as a potential new avenue for pest control, and in parallel, to understand the differential ability of mites to feed on a wide plants hosts. To determine factors that contribute most to crop success/failure within the changing agricultural ecosystem is essential to develop strategies to mitigate pest damage and increase plant performance. Our team, within the GAP-M consortium (Genomics in Agriculture Pest Management), participates in the development of genomic and histological tools derived from the plant-spider mite interplay, including whole genome sequences and annotations of T. urticae and databases for transcriptome and metabolome responses in both, plant and mite, sides of the interaction (Santamaria et al. 2012; 2013; 2015; 2018; Zhurov et al. 2014; Martel et al. 2015; Ojeda-Martinez et al., 2020; 2021). Besides, our group has identified and characterized some plant genes as candidates for pest control in the reciprocal whole genome studies in plant-pest interactions (Santamaria et al. 2013; 2017; 2018; 2019; Arnaiz et al. 2018; 2019, 2021).

 

  
 

Recently, we have expanded our scope to other arthropod herbivores. Starting from a set of 28 Arabidopsis-herbivore transcriptomic experiments, we performed a bioinformatics comprehensive analysis to discover novel pathways involved in the response of the plant to T. urticae (Santamaria et al., 2021), as well as to disentangle specificities and commonalities in plant/pest interactions (Garcia et al., 2021). These results are highly relevant to understand step by step the whole pathway, from the herbivore detection, the signal transduction or the hormonal related crosstalk, to culminate in specific plant defence responses. The analysis of the perception, signalling and transmission of alarms between cells and to other parts of the damaged plant is currently the main focus of our research. The final goal is to understand how plants (models and crops) respond to herbivory.

2. Understanding the effects of environmental conditions on plant-pest interactions.

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 are expected to have profound effects on the plant-herbivore interactions. These intricate interactions can be dissected only using novel technologies that can relate interactions at the genome and metabolome level as a function of climate change parameters and linking them to fitness outputs for these organisms. This 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.


 

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. Our group has determined the role of several pathways and genes in the interaction of Arabidopsis plants with spider mites, covering different aspects including plant perception, signal transduction and end responses (reviewed in Santamaria et al., 2020). To a better understanding of the molecular pathways, our analyses will be extended to a second herbivore, the insect Pieris brassicae, and to crop plants such are Solanum lycopersicum, Brassica rapa and Phaseolus vulgaris. In this context, our main goals are to know how the molecular signalling is modified upon a particular herbivore attack and how climate change affects these interactions.

Representative Publications

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

Velasco-Arroyo, B., Martinez, M., Diaz, I., Diaz-Mendoza, M. 2018. Differential response of silencing HvIcy2 barley plants against Magnaporthe oryzae infection and light deprivation. BMC Plant Biology 18, 337. DOI: 10.1186/s12870-018-1560-6

Gomez-Sanchez, A., Gonzalez-Melendi, P., Santamaria, M.E., Arbona, V., Lopez-Gonzalvez, A., Garcia, A., Hensel, G., Kumlehn, J., Martinez, M., Diaz, I. 2018. Knock-downs for drought-induced cysteine-protease genes alter barley leaf structure and the response to abiotic and biotic stresses. Journal of Experimental Botany ery410. DOI: 10.1093/jxb/ery410

Arnaiz, A; Talavera-Mateo, L; Gonzalez-Melendi, P; Martinez, M; Diaz, I; Santamaria, ME. 2018. "Arabidopsis Kunitz trypsin inhibitors in defense against spider mites". Frontiers in Plant Science. DOI: 10.3389/fpls.2018.00986".

Santamaría, ME; 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. DOI: 10.1038/s41598-018-27904-1".

Santamaria, ME; Arnaiz, A; Gonzalez-Melendi, P; Martinez, M; Diaz, I. 2018. "Plant perception and short-term responses to phytophagous insects and mites". International Journal of Molecular Sciences. DOI: 10.3390/ijms19051356".

Santamaria, ME; Diaz, I; Martinez, M. 2018. "Dehydration stress contributes to the enhancement of plant defense response and mite performance on barley". Frontiers in Plant Science. DOI: 10.3389/fpls.2018.00458".

Santamaria, M; Diaz-Mendoza, M; Perez-Herguedas, D; Hensel, G; Kumlehn, J; Diaz, I; Martinez, M. 2018. "Overexpression of HvIcy6 in barley enhances resistance against Tetranychus urticae and entails partial transcriptomic reprogramming". International Journal of Molecular Sciences. DOI: 10.3390/ijms19030697".

Velasco-Arroyo B, Diaz-Mendoza M, Gomez-Sanchez A, Moreno-Garcia B, Santamaria ME, Torija-Bonilla M, Hensel G, Kumlehn J, Martinez M, Diaz I. 2018. "Silencing barley cystatins HvCPI-2 and HvCPI-4 specifically modifies leaf responses to drought stress". Plant Cell Environ. DOI: 10.1111/pce.13178".

Bárány, I; Berenguer, E; Solís, M-T; Pérez-Pérez, Y; Santamaría, ME; Crespo, J-L; Risueño, MC; Díaz, I; Testillano, PS. 2018. "Autophagy is activated and involved in cell death with participation of cathepsins during stress-induced microspore embryogenesis in barley". Journal of Experimental Botany. DOI: 10.1093/jxb/erx455".

Alonso, J; Martinez, M. 2017. "Insights into the molecular evolution of peptidase inhibitors in arthropods". PLoS One. DOI: 10.1371/journal.pone.0187643".

Diaz-Mendoza, M; Velasco-Arroyo, B; Santamaria, ME; Diaz, I; Martinez, M. 2017. "HvPap-1 C1A protease participates differentially in the barley response to a pathogen and an herbivore". Frontiers in Plant Science. DOI: 10.3389/fpls.2017.01585".

Radchuk, V; Tran, V; Radchuk, R; Diaz-Mendoza, M; Weier, D; Fuchs, J; Riewe, D; Hensel, G; Kumlehn, J; Munz, E; Heinzel, N; Rolletschek, H; Martinez, M; Borisjuk, L. 2017. "Vacuolar processing enzyme 4 contributes to maternal control of grain size in barley by executing programmed cell death in the pericarp". New Phytologist. DOI: 10.1111/nph.14729".

Santamaría, ME; 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. DOI: 10.3389/fpls.2017.00975".

Santamaría, ME; Auger, P; Martínez, M; Migeon, A; Castañera, P; Díaz, I; Navajas, M; Ortego, F. 2017. "Host plant use by two distinct lineages of the tomato red spider mite, Tetranychus evansi, differing in their distribution range". Journal of Pest Science. DOI: 10.1007/s10340-017-0852-1".

Velasco-Arroyo, B; Diaz-Mendoza, M; Santamaria, ME; Gonzalez-Melendi, P; Gomez-Sanchez, A; Arnaiz, A; Martinez, M; Diaz, I. 2017. "Senescence-associated genes in response to abiotic/biotic stresses", p. 1-21, Progress in Botany. Springer Berlin Heidelberg, Berlin, Heidelberg. DOI: 10.1007/124_2017_1".

Diaz-Mendoza, M; Dominguez-Figueroa, J; Velasco-Arroyo, B; Cambra, I; Gonzalez-Melendi, P; Lopez-Gonzalvez, A; Garcia, A; Hensel, G; Kumlehn, J; Diaz, I; Martinez, M. 2016. "HvPap-1 C1A protease and HvCPI-2 cystatin contribute to barley grain filling and germination". Plant Physiology. DOI: 10.1104/pp.15.01944".

Martinez, M. 2016. "Computational tools for genomic studies in plants". Current Genomics. Volume 17, Number 6, pp. 509-514

Martinez, M; Santamaria, M; Diaz-Mendoza, M; Arnaiz, A; Carrillo, L; Ortego, F; Diaz, I. 2016. "Phytocystatins: Defense Proteins against Phytophagous Insects and Acari". International Journal of Molecular Sciences. DOI: 10.3390/ijms17101747".

Diaz-Mendoza, M; Velasco-Arroyo, B; Santamaria, ME; González-Melendi, P; Martinez, M; Diaz, I. 2016. "Plant senescence and proteolysis: two processes with one destiny". Genetics and Molecular Biology. DOI: 10.1590/1678-4685-GMB-2016-0015".

Bensoussan, N; Santamaria, ME; Zhurov, V; Diaz, I; Grbic, M; Grbic, V. 2016. "Plant-herbivore interaction: dissection of the cellular pattern of Tetranychus urticae feeding on the host plant". Frontiers in Plant Science. DOI: 10.3389/fpls.2016.01105".

Velasco-Arroyo, B; Diaz-Mendoza, M; Gandullo, J; Gonzalez-Melendi, P; Santamaria, ME; Dominguez-Figueroa, JD; Hensel, G; Martinez, M; Kumlehn, J; Diaz, I. 2016. "HvPap-1 C1A protease actively participates in barley proteolysis mediated by abiotic stresses". Journal of Experimental Botany. DOI: 10.1093/jxb/erw212".

Abraham, Z; Iglesias Fernández, R; Martinez, M; Diaz, I; Carbonero, P; Vicente-Carbajosa, J. 2016. "A developmental switch of gene expression in the barley seed mediated by HvVP1 (Viviparous1) and HvGAMYB interactions". Plant Physiology. DOI: 10.1104/pp.16.00092".

Garzo, E; Moreno, A; Hernando, S; Mariño, V; Torne, M; Santamaria, ME; Díaz, I; Fereres, A. 2015. "Electrical Penetration Graph technique as a tool to monitor early stages of aphid resistance to insecticides". Pest Management Science. DOI: 10.1002/ps.4041".

Santamaria, ME; Arnaiz, A; Diaz-Mendoza, M; Martinez, M; Diaz, I. 2015. "Inhibitory properties of cysteine protease pro-peptides from barley confer resistance to spider mite feeding". PLoS One. DOI: 10.1371/journal.pone.0128323".

Santamaría, ME; González-Cabrera, J; Martínez, M; Grbic, V; Castañera, P; Díaz, l; Ortego, F. 2015. "Digestive proteases in bodies and faeces of the two-spotted spider mite, Tetranychus urticae". Journal of Insect Physiology. DOI: http://dx.doi.org/10.1016/j.jinsphys.2015.05.002".

Martel, C; Zhurov, V; Navarro, M; Martinez, M; Cazaux, M; Auger, P; Migeon, A; Santamaria, ME; Wybouw, N; Diaz, I; Van Leeuwen, T; Navajas, M; Grbic, M; Grbic, V. 2015. "Tomato Whole Genome Transcriptional Response to Tetranychus urticae Identifies Divergence of Spider Mite-Induced Responses Between Tomato and Arabidopsis". Molecular Plant-Microbe Interactions. DOI: 10.1094/MPMI-09-14-0291-FI".

Zhurov, V; Navarro, M; Bruinsma, KA; Arbona, V; Santamaria, ME; Cazaux, M; Wybouw, N; Osborne, EJ; 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, RM; Van Leeuwen, T; Grbić, V. 2014. "Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding Chelicerate herbivore spider mite". Plant Physiology. DOI: 10.1104/pp.113.231555".

Diaz-Mendoza, M; Velasco-Arroyo, B; González-Melendi, P; Martinez, M; Diaz, I. 2014. "C1A cysteine protease–cystatin interactions in leaf senescence". Journal of Experimental Botany. DOI: 10.1093/jxb/eru043".

Santamaría, ME; Diaz-Mendoza, M; Diaz, I; Martinez, M. 2014. "Plant protein peptidase inhibitors: an evolutionary overview based on comparative genomics". BMC Genomics. DOI: 10.1186/1471-2164-15-812".

Julián, I; Gandullo, J; Santos-Silva, LK; Diaz, I; Martinez, M. 2013. "Phylogenetically distant barley legumains have a role in both seed and vegetative tissues". Journal of Experimental Botany. DOI: ert132 [pii] 10.1093/jxb/ert132".

Santamaria, ME; Martinez, M; Cambra, I; Grbic, V; Diaz, I. 2013. "Understanding plant defence responses against herbivore attacks: an essential first step towards the development of sustainable resistance against pests". Transgenic Research. DOI: 10.1007/s11248-013-9725-4".

Cambra, I.; Hernández, D.; Diaz, I.; Martinez, M. 2012. Structural basis for specificity of propeptide-enzyme interaction in barley C1A cysteine peptidases. PLoS One 7:e37234.

Martinez, M.; Cambra, I.; Gonzalez-Melendi, P.; Santamaria, M.E.; Diaz, I. 2012. C1A cysteine-proteases and their inhibitors in plants. Physiologia Plantarum 145:85-94.

Diaz, I.; Santamaria, M.E. 2012. "Biotechnological approaches to combat phytophagous arthropods. In: Arthropod-Plant interactions: novel insights and approaches for IPM. Series: Progress in Biological Control", Vol. 14. Smagghe, G. and Diaz, I. (Eds.) Springer, Dordrecht, Heidelberg, New York, London. p. 6-14

Martinez, M.2012. "Co-evolution of genes for specification in arthropod-plant interactions: a bioinformatic analysis in plant and arthropod genomes. In: Arthropod-Plant interactions: novel insights and approaches for IPM. Series: Progress in Biological Control", Vol. 14. Smagghe, G. and Diaz, I. (Eds.) Springer, Dordrecht, Heidelberg, New York, London. p. 1-14

Martinez, M.; Dáder, B.; González-Melendi, P.; Gandullo, J.; Santamaria, M.E.; Diaz, I. 2012. A cathepsin F-like peptidase involved in barley grain protein mobilization, HvPap-1, is modulated by its own propeptide and by cystatins. Journal of Experimental Botany 63:4615-4629.

Santamaria, M.E.; Hernández-Crespo, P.; Ortego, F.; Grbic, V.; Grbic, M.; Diaz, I.; Martinez, M. 2012. Cysteine peptidases and their inhibitors in Tetranychus urticae: a comparative genomic approach. BMC Genomics 13:307.

Santamaria, M.E.;Cambra, I.;Martinez, M.; Pozancos, C.; González-Melendi, P.; Grbic, V.; Castañera, P.; Ortego, F.; Diaz, I. 2012. Gene pyramiding of peptidase inhibitors enhances plant resistance to the spider mite Tetranychus urticae. PLoS One 7:e43011

Spider mite damage quantification method
 
 
 
 
 
 
 
 
 

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