MOLECULAR PLANT-PEST INTERACTIONS
- Contreras Navarro, Estefanía - Postdoctoral Fellow
- García García, Alejandro - PhD Student
- Martínez Muñoz, Manuel - Associate Professor
- Ojeda Martínez, Dairon Antonio - PhD Student
- Romero Hernandez, Gara - PhD Student
- Rosa Díaz, Irene - PhD Student
- Santamaría Fernández, Estrella - Ramón y Cajal fellow
The group is involved in two research lines focused on:
- Deciphering of the plant defense responses to spider mite infestations.
- Analyze the role of C1A cysteine-proteases in the protein degradation/mobilization events mediated by biotic/abiotic stresses and crop productivity.
- Computational approaches on defense-related gene families.
1) Deciphering of the plant defense responses to spider mite infestation.
The two-spotted spider mite Tetranychus urticae is a cosmopolitan agricultural acari, 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, causing damages approaching 1 billion dollars worldwide. Another spider mite species extremely invasive is T. evansi, a pest of recent introduction from South America in the EU agriculture, which only infests Solanaceae species. 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. 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 research tries to understand the differential ability of mites to feed on a wide or narrow plant host, to decode the plant defense responses (genes, signaling 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 acari-pest control.
Tetranychus urticae feeding on bean.
Scheme of plants responses to spider mite feeding.
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. The development of new tools is essential for an efficient and environmentally-friendly spider mite pest management under conditions of changing climate. Our team, within the GAP-M consortium (Genomics in Agriculture Pest Management), participates in the development of genomic tools and databases derived from the plant-spider mite interplay, including whole genome sequences and annotations of T. urticae and T. evansi and databases for transcriptome and metabolome responses in both, plant and mite, sides of the interaction (Grbic et al. 2011; Santamaria et al. 2012; 2013; 2015; 2018; Zhurov et al. 2014, Martel et al. 2015). 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; Arnaiz et al. 2018). These results are highly relevant to understand step by step the whole pathway, from the mite detection, the signal transduction or the hormonal related crosstalk, to culminate in specific plant defense responses. The analysis of the perception, signaling 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 spider mite feeding, oviposition and frass deposition.
2) Analyze the role of C1A cysteine-proteases in the protein degradation/mobilization events mediated by biotic/abiotic stresses and crop productivity.
Plants defend themselves of adverse condition by activating an orchestrated molecular network highly regulated that triggers molecular, biochemical, physiological and morphological changes to minimize damage. High protease activities are closely associated with abiotic stresses, enhancing the protein turn-over required for metabolic processes and nutrient recycling. We study the roles of barley C1A cysteine-proteases and cystatins, specific inhibitors of their proteolytic activities, that exert a complex regulatory role in this physiological process. We try to clarify the association between protein degradation and mobilization events mediated by biotic/abiotic stresses and the alterations of yield crop and its nutritional value. Understanding the complex mechanisms that exist in the stress-induced senescence should facilitate the creation of strategies and technologies for the improvement of cereal crops.
Phenotypical, biochemical and physiological behavior of barley plants throughout the natural lifespan. Sg: stomatal conductance. w: weeks of development.
Our results, derived from the study on barley cysteine-proteases and their modulators, have demonstrated that abiotic (drought, nitrogen starvation or darkness) and biotic (spider mite feeding) stresses modified gene expression patterns and accelerated barley leaf senescence by triggering the chlorophyll loss with the subsequent reduction of photosynthesis, degradation of macromolecules and dismantling of cellular components (Diaz-Mendoza et al. 2014; Velasco-Arroyo et al. 2016). The analysis of the cysteine-proteases/cystatin expression, location and activity under different stresses has shown: i) a functional specificity of proteases and cystatins depending on the stress; ii) in some cases a cooperative role among them; and iii) important effects on plant lifespan. The generation of transgenic barley lines over-expressing or silencing protease or cystatin genes has allowed not only to get wider knowledge on its physiology, but also to obtain stay-green phenotypes, lines with alterations in the grain filling and consequently delayed in the grain germination, and even barley lines with thicker leaf cuticles and higher protection against pathogens and pests (Diaz-Mendoza et al. 2016; 2017; Gomez-Sanchez et al. 2018; Santamaria et al. 2018; Velasco-Arroyo et al. 2018). These findings highlight the potential of the biotechnological manipulation to control the timing of plant growth and the plant survival under abiotic and biotic conditions.
3) Computational approaches on defense-related gene families.
The main objective of this line is the in silico prediction and analysis of gene families involved in plant defense mechanisms. For that, comparative genomics is a key tool since it permits to predict the existence and the number of members of each gene family in different species (Martinez 2011; 2013; 2016). Using bioinformatics tools and genomic databases, evolutionary and phylogenetic analyses have been made in order to identify species-specific proteins involved in pest and pathogen resistance, and to determine the sequence variations that could explain their specific role (Santamaria et al. 2014; Alonso and Martinez 2017). Currently, we are focused in the integration of genomic, transcriptomic and metabolomic data to determine protein networks involving gene families in defense signaling.
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