Group leader: Isabel Díaz Rodríguez - Professor

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The research lines of the group are focused on:
  1. Plant defense responses to spider mite feeding.
  2. Protein degradation/mobilization events during barley leaf senescence.
  3. Phylogeny and evolution of plant defense genes.
1) Plant defense responses to spider mite feeding

The two-spotted spider mite Tetranychus urticae is a cosmopolitan agricultural acari pest feeding on over 1,100 different plants, 150 of them of agricultural importance, causing damages approaching 1 billion dollars worldwide. In addition, another spider mite species extremely invasive is T. evansi which only feed Solanaceae species, a pest of recent introduction from South America in the EU agriculture. Due to high fecundity, inbreeding and short generation time Tetranychidae populations develop resistance to acaricides after one to four years of use. Our research tries to understand the differential ability of mites to feed on a wide or narrow plant host, to decode the plant responses (genes and signaling pathways) that confer resistance to mites and to apply the knowledge gained through basic science as a potential new avenue for acari-pest control.

T. urticae and T. evansi and their silks on bean and tomato, respectively


Climate change, in particular increased temperatures and drought, clearly favour feeding pest development and it is expected that spider mites will expand their natural range. The effect of changing climate on plant and spider mite physiology and plant-spider mite interaction is still unknown. 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 project gained at the FACCE-ERA-NET call will allow our team, as member of the GAP-M consortium (Genomics in Agriculture Pest Management), the identification and analysis of the critical parameters, and the development of new tools for efficient and environmentally-friendly spider mite pest management under conditions of changing climate.

Our team, within the GAP-M consortium, has participated in the development of genomic/proteomic tools and databases for spider mite pests including: whole genome sequences and annotations of T. urticae, T. evansi and T. lintearius, expression microarray to monitor transcriptional changes, databases of transcriptome and proteome responses to developmental stages and host changes for both T. urticae and T. evansi (Grbic et al. 2011; Santamaria et al. 2012a,b; 2013; Zhurov et al. 2014; Santamaria et al., 2015a). Our group has identified several genes as candidates for pest control in the reciprocal whole genome studies in plant-pest interactions between spider mites and Arabidopsis and tomato plants (Zhurov et al. 2014; Martel et al. 2015). We are characterizing some of these genes that participate in the intracellular signaling cascade to trigger host resistance to spider mites. These results are highly relevant to understand the steps of the signal transduction pathway induced by the spider mite that culminate in specific plant defense responses, the transmission of alarms to cells in other parts of the damaged plant or even to send alerts to neighbor plants. 

2) Protein degradation/mobilization events during barley leaf senescence

High nutrient mobilization efficiency is an intrinsic feature of plant senescence. This complex process involves a well-orchestrated activation of genes encoding catabolic enzymes, among others, to remobilize nutrients, in particular nitrogen, from the senescing organs to still growing plant parts, and finally to the developing seeds. Each senescing-promoting factor (abiotic/biotic) up-regulates a subset of senescence-associated genes (SAGs), many of them encoding proteases with a crucial role in nutrient recycling.

The massive net degradation of proteins involves broad metabolic networks, different subcellular compartments, and several types of proteases and regulators. We study the roles of barley C1A cysteine-proteases, the most abundant enzymes responsible for the proteolytic activity during leaf senescence as well as the role of cystatins, specific modulators of C1A peptidase activities that exert a complex regulatory role in this physiological process. We try to clarify the association between protein degradation/mobilization events mediated by biotic/abiotic stresses and their consequences on crop yield and quality. Understanding complex mechanisms in the stress-induced senescence should facilitate the creation of strategies and technologies for the improvement of crops.

The most important results derived from our studies on barley cysteine-proteases and their modulators in the leaf senescence have demonstrated that, besides senescence-mediated by abiotic stresses such nitrogen starvation or darkness, the spider mite T. urticae feeding has a potential impact and accelerates barley leaf senescence. Both abiotic and biotic stresses trigger the chlorophyll loss with the subsequent reduction of photosynthesis, degradation of macromolecules and dismantling of cellular components (Martinez et al. 2012; Diaz and Martinez 2013). The analysis of the cysteine-proteases/cystatin expression and location under different stress conditions, have allowed the determination of functional specificity of proteases and cystatins depending on the stress treatment (Cambra et al. 2012b; Diaz-Mendoza et al. 2014). Currently, we are studying the leaf senescence behavior of transgenic barley lines over-expressing or silencing protease or cystatin genes, under abiotic (darkness and drought) and biotic (spider mite feeding) conditions. First results corroborate the important role of proteolytic events in nutrient recycling and support the potential of biotechnology to modulate proteolysis in order to obtain higher grain yield (Diaz-Mendoza et al. 2016; Velasco-Arroyo et al., 2016).

3) Comparative genomics of gene families involved in plant-pest interactions.

The main objective of this line is to know the origin and evolution of different gene families involved in plant defense mechanisms and in pest attack. Comparative genomics analyses of protein families are based in current bioinformatics tools and genomic databases (Martinez 2011, 2013, 2016). These analyses are performed to determine the existence and the number of members of each family in different clades. With these sequences, phylogenetic analyses are made in order to identify species-specific proteins involved in plant resistance and pest attack, and to determine the sequence variations that could explain their specific role (Cambra et al. 2012a; Santamaria et al. 2014).

Research Projects
  • New generation sustainable tools to control emerging mite pests under climate change. FACCE-ERA- NET, EU, 2014-17. IP: I Diaz (Coordinator: J Cross-UK)
  • Identificación de genes de resistencia en poblaciones de áfidos. DOW AGROSCIENCES IBERICA, 2014. IP: I Diaz.
  • Estudio del efecto de compuestos de origen vegetal frente a artrópodos fitófagos. SEIPASA, 2013-14. IP: I Diaz.
  • Cisteín-proteasas de cebada: caracterización fisiológica de proteasas tipo papaína en funciones endógenas y defensa. MINECO, 2012-14. IP: I Diaz.
  • Propéptidos como moléculas de defensa en plantas. Aproximaciones biotecnológicas. UPM-CAM, 2011. IP: M Martinez.
  • Pest genomics plant breeding in a sustainable agricultural pest management. ONTARIO MINISTRY OF RESEARCH AND INNOVATION, Canada, 2010-13. IP: I Diaz (Coordinator: M. Grbic-Canadá)

Representative Publications

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:".

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

Cambra, I.; 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


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