SIGNALING NETWORKS IN PLANT RESPONSES TO NITROGEN AND SULPHUR LIMITATION

Group leader: Joaquín Medina Alcázar - Researcher CSIC-INIA
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Personnel:

 



1-Summary

“The main objective of our research is to understand the genetic and molecular mechanisms involved in plant adaptation”.

The main goal of our research is to understand how primary nitrogen and sulphur metabolism is regulated and coordinated and how they modulate growth and development. We are especially interested in the way other adverse environmental conditions like extreme temperatures and drought modulate nutrient status and nutrient stress responses. We are conducting different high throughput genetic strategies, developing system biology tools, and a set of growth conditions to dissect the signalling pathways and the molecular and genetic mechanisms involved in the control of the nutrient status on growth and development. Arabidopsis and tomato and their relative wild species are used as models in the different research lines.


2-Background

In nature, plants usually grow in soil that contains very low amounts of macronutrients like Nitrogen and Sulphur or might suffer from an unbalanced proportion of both macronutrients. To adapt and grow in nutrient-deprived environments, plants have developed sophisticated strategies and molecular mechanisms to cope with different nutrient limitations. In fact, when plants have to deal with limitation of a specific nutrient, the metabolism of other nutrients will be adjusted to maintain proper growth and development. Besides, different studies suggested that the balance between nitrogen (N), sulphur (S) and carbon (C) rather than one single metabolite, affects global gene expression. In addition, cellular C and N/S metabolism is closely coordinated for C-N-S-containing metabolite synthesis at the biochemical level and also for long-distance sensing and signalling of the C/N and S balance. Transcriptomic analysis suggested that both N and S starvation and N or S-resupply after starvation affect many genes involved in C or N-S metabolism. Despite all genome-wide gene expression analyses, the mechanisms underlying the crosstalk among C, N and S metabolic pathways is unclear, as is the crosstalk of C, N and S with other nutrient metabolic pathways and only a few regulators have been identified.


 

  

3-Objectives

Our main goal is to understand how nitrogen and Sulphur signalling pathways crosstalk with other signalling networks to control plant growth and development. This is a key element for improving nitrogen and sulphur use efficiency in crops, or improves biomass production and fruit and seed quality which are very serious issues in modern agriculture. Recently, we develop different genetic screenings together with network models in Arabidopsis and tomato and identified new regulators and networks modules, which are controlled by nitrogen & sulphur nutritional status. Our work indicates the possibility of different regulatory links between water and temperature stress responses and nitrogen and sulphur metabolism in Arabidopsis and tomato. However, the specific function and the molecular mechanisms are poorly understood. To answer these questions, we will use a multiple strategy that involves: A) development of a platform for large scale genetic screenings and functional studies of the selected candidate genes, B) Integrated bioinformatics tools to generate gene/metabolite networks models and selection of the most important regulatory genes and C) functional genomics and natural variation analyses for the characterization of the mutant phenotypes. The multiple approaches will help to understand the complex molecular mechanisms that operate in the crosstalk between N-S nutrient signalling pathways.


Our lab has 3 main objectives of research:

1-System analyses of Plant Nitrogen & Sulphur metabolism.


Our research interests can be divided into 2 interconnected aims:

- We are looking for regulatory components involved in nitrate and sulphate signalling pathways. Especially we are interested in the ones that would help us to understand local and systemic responses to S/N nutritional status.

- We try to understand the molecular events that connect nutrient stress signalling and hormone signalling to responses to other environmental stress conditions like drought or extreme temperatures, which often limit nutrient uptake and assimilation.


Figure. Gene Co-expression Network Analysis predicts New Candidate Genes and Functional Modules Involved in the Sulphate Response (Henriquez-Valencia et al 2018).


Figure. General strategy to identify regulators involved in N/S nutritional responses.

 

 

2-Environmental genomics and computational modelling the Interaction of plants and root associated bacteria enhancing plant mineral nutrition.

We are the studying the nutritional responses of plants species living in extreme environments which includes the ones growing in nutrient poor-soils or hyper-arid, arid and semi-arid regions like the Atacama Desert in Chile. The main goal is to identify specific adaptations, new strategies, biochemical pathways and genes that allow plants to live in such extreme conditions. In collaboration with Drs Mauricio Gonzalez, Rodrigo Gutierrez and Mark Wilkinson, we are analysing the structure and dynamics of the plant-associated soil microbiome as it responds to natural and applied perturbations.


Figure. Map of northern Chile showing location of the Salar de Atacama and adjacent Andes (right inset) and a digital model indicating sampling sites (lower inset, coloured dots) along the Talabre-Lejía Transect (Diaz et al 2016).

 

 

 3-Improve nutrient use efficiency in crops.

Up to now, most crop varieties have been selected and domesticated under non-limiting Nutrient conditions. To reduce the excessive input of fertilizers without affecting plant growth and productivity it is crucial to improve both Nutrient uptake and assimilation of plants under low or moderate Nutrient supply. Actually, our objective is to obtain new crops with enhanced Nutrient use efficiency (NUE). We are using genetic approaches based on utilizing existing natural variation for NUE traits in a crop model like tomato. In addition, we are designing different molecular strategies for transferring the identified nutritional-related regulatory modules in different crops such as cereals or solanaceae species.


Figure. Overexpression of CDF3 in tomato improves yield and fruit size in control and salt stress conditions (Renau-Morata et al 2017).

 

 

4-Main lines of research:

  1. Nitrate and sulphate signalling
  2. Role of Nutrient remobilization and Autophagy in abiotic stress tolerance
  3. Study Nutritional responses of plants adapted to oligotrophic environments: Atacama plants species
  4. Improve nutrient use efficiency in crops: Tomato /cereals
Estudiantes Master, TFG o Practicas

  1. Alejandro Quin Minguela
  2. Cristina González Izquierdo
  3. Ahmad Razavizadeh
  4. Benhan Mondak
  5. Pablo Orestes Rojas
  6. Lissette Ulloa Zepeda
  7. Juan Donaldo Dueñas Pérez
  8. Alba Hernangómez Laderas TFG
  9. Alexandre Tselykh
  10. Laura Figueruela Asencio
  11. Sara Vives Rodriguez
  12. Marisa Delgado Dolset
  13. Alicia Mata
  14. Elena Sánchez
  15. Ignacio Sánchez
  16. Mildred Ocampo
  17. Diana Andrea Gil
  18. Cruz Enrique Beltrán
  19. Blanca Aridai
  20. Javier Gloazzo

Proyectos

  1. Molecular analyses of Nitrogen responses in tomato genotypes with contrasting NUE (2021-2024)
  2. 2019-2023. Acronym: VEG-ADAPT. EU PRIMA. “Adapting Mediterranean vegetable crops to climate change-induced multiple stresses”.
  3. 2018-2020. SO-CBGP-EoI2017 CBGP Program Severo Ochoa. “Spatio temporal changes in the plant associated soil microbiome and their association with plant health and sustainable agriculture”. PIs Mark Wilkinson and Joaquin Medina.
  4. CA15138 COST (2017-20) “TRANSAUTOPHAGY: European Network of Multidisciplinary Research and Translation of Autophagy knowledge
  5. REDI170024. CONICYT. (2017-2019). “RINAP” Red Iberoamericana de la Nutrición de Azufre en Plantas”. IPs Joaquín Medina Alcázar, Javier Canales
  6. RTA2015-00014-c02-00 (2017-20) Improvement of tomato production through increased carbon assimilation and nitrogen use efficiency using transcription regulators IP Joaquín Medina
  7. PUC1566 (2016-2017). Internationalization Program PUC, (Pontificia Universidad Católica de Chile). New strategies for the improvement of crops under conditions of climate change: Identification of new genes involved in the assimilation of micro-nutrients. IP Dr. Diego Goméz Cassati, Dr. Catherine Curie. Dr. Hannetz Roschzttardtz. Dr Jesus Vicente. Dr Joaquin Medina
  8. RTA2012-00008-CO2 (2013-2016). “Utilización de factores transcripcionales como herramienta para incrementar la producción de biomasa y la tolerancia a estreses abióticos en solanáceas”. IP Joaquín Medina.
  9. Proyecto Explora 2015-17. Aumento en la captura de energía y carbono en sistemas vegetales. IP Jesús Vicente.
  10. OPTISOL. Optimized lignocellulose exploitation from solanaceae canopy. Inspire Program. IP Stephan Pollmann
  11. AECID A1/039269/11 (2011-2014). Fortalecimiento científico e institucional para el desarrollo de la biotecnología en la UNASAM (HUARAZ, PERÚ) a través de la colaboración con el centro de biotecnología y genómica de plantas (CBGP, UPM-INIA).
  12. RTA2009-00042-CO2-01 (2009-2012). Desarrollo de nuevas estrategias para la mejora de la resistencia a condiciones de estrés abiótico en tomate mediante la utilización de genes reguladores.
  13. CGL2009-13429-C02-01 (2008-2011). Diversidad en las algas liquénicas del género Trebouxia: Caracterización fenotípica y molecular.
  14. AT08-002 (2008-2009). Estudio del desarrollo de la semilla como fuente de nuevas estrategias para la obtención de plantas tolerantes a condiciones ambientales extremas

 


Representative Publications

Mandakovic, D., Aguado-Norese, C., García-Jiménez, B., Hodar, C., Maldonado, J.E., Gaete, A., Latorre, M., Wilkinson, M.D., Gutiérrez, R.A., Cavieres, L.A., Medina, J., Cambiazo, V., Gonzalez, M. 2023. Testing the stress gradient hypothesis in soil bacterial communities associated with vegetation belts in the Andean Atacama Desert. Environmental Microbiome 18, 24. DOI: 10.1186/s40793-023-00486-w

Carrillo, L., Baroja-Fernández, E., Renau-Morata, B., Muñoz, F.J., Canales, J., Ciordia, S., Yang, L., Sánchez-López, Á.M., Nebauer, S.G., Ceballos, M.G., Vicente-Carbajosa, J., Molina, R.V., Pozueta-Romero, J., Medina, J. 2023. Ectopic expression of the AtCDF1 transcription factor in potato enhances tuber starch and amino acid contents and yield under open field conditions. Frontiers in Plant Science 14. DOI: 10.3389/fpls.2023.1010669

Canales, J., Arenas-M, A., Medina, J., Vidal, E.A. 2023. A Revised View of the LSU Gene Family: New Functions in Plant Stress Responses and Phytohormone Signaling. International Journal of Molecular Sciences 24, 2819. DOI: 10.3390/ijms24032819

Uribe, F., Henríquez-Valencia, C., Arenas-M, A., Medina, J., Vidal, E.A., Canales, J. 2022. Evolutionary and Gene Expression Analyses Reveal New Insights into the Role of LSU Gene-Family in Plant Responses to Sulfate-Deficiency. Plants 11, 1526. DOI: 10.3390/plants11121526

Contreras-López, O., Vidal, E.A., Riveras, E., Alvarez, J.M., Moyano, T.C., Sparks, E.E., Medina, J., Pasquino, A., Benfey, P.N., Coruzzi, G.M., Gutiérrez, R.A. 2022. Spatiotemporal analysis identifies ABF2 and ABF3 as key hubs of endodermal response to nitrate. Proceedings of the National Academy of Sciences 119. DOI: 10.1073/pnas.2107879119

Renau-Morata, B., Molina, R.-V., Minguet, E.G., Cebolla-Cornejo, J., Carrillo, L., Martí, R., García-Carpintero, V., Jiménez-Benavente, E., Yang, L., Cañizares, J., Canales, J., Medina, J., Nebauer, S.G. 2021. Integrative Transcriptomic and Metabolomic Analysis at Organ Scale Reveals Gene Modules Involved in the Responses to Suboptimal Nitrogen Supply in Tomato. Agronomy 11, 1320. DOI: 10.3390/agronomy11071320

García-Jiménez, B., Muñoz, J., Cabello, S., Medina, J., Wilkinson, M.D. 2020. Predicting microbiomes through a deep latent space. Bioinformatics. DOI: 10.1093/bioinformatics/btaa971

Domínguez-Figueroa, J., Carrillo, L., Renau-Morata, B., Yang, L., Molina, R.-V., Marino, D., Canales, J., Weih, M., Vicente-Carbajosa, J., Nebauer, S.G., Medina, J. 2020. The Arabidopsis Transcription Factor CDF3 Is Involved in Nitrogen Responses and Improves Nitrogen Use Efficiency in Tomato. Frontiers in Plant Science 11, 1825. DOI: 10.3389/fpls.2020.601558

Coleto, I., Bejarano, I., Marín‐Peña, A.J., Medina, J., Rioja, C., Burow, M., Marino, D. 2020. Arabidopsis thaliana transcription factors MYB28 AND MYB29 shape ammonium stress responses by regulating fe homeostasis. New Phytologist. DOI: 10.1111/nph.16918

Canales, J., Uribe, F., Henríquez-Valencia, C., Lovazzano, C., Medina, J., Vidal, E.A. 2020. Transcriptomic analysis at organ and time scale reveals gene regulatory networks controlling the sulfate starvation response of Solanum lycopersicum. BMC Plant Biology 20, 385. DOI: 10.1186/s12870-020-02590-2

Renau-Morata, B., Carrillo, L., Cebolla-Cornejo, J., Molina, R.V., Martí, R., Domínguez-Figueroa, J., Vicente-Carbajosa, J., Medina, J., Nebauer, S.G. 2020. The targeted overexpression of SlCDF4 in the fruit enhances tomato size and yield involving gibberellin signalling. Scientific Reports 10, 10645. DOI: 10.1038/s41598-020-67537-x

Renau-Morata, B., Carrillo, L., Dominguez-Figueroa, J., Vicente-Carbajosa, J., Molina, R.V., G. Nebauer, S., Medina, J. 2020. CDF transcription factors: plant regulators to deal with extreme environmental conditions. Journal of Experimental Botany. DOI: 10.1093/jxb/eraa088

Alvarez, J.M., Moyano, T.C., Zhang, T., Gras, D.E., Herrera, F.J., Araus, V., O’Brien, J.A., Carrillo, L., Medina, J., Vicente-Carbajosa, J., Jiang, J., Gutiérrez, R.A. 2019. Local Changes in Chromatin Accessibility and Transcriptional Networks Underlying the Nitrate Response in Arabidopsis Roots. Molecular Plant. DOI: 10.1016/j.molp.2019.09.002

Arraño-Salinas, P; Domínguez-Figueroa, J; Herrera-Vásquez, A; Zavala, D; Medina, J; Vicente-Carbajosa, J; Meneses, C; Canessa, P; Moreno, AA; Blanco-Herrera, F. 2018. "WRKY7, -11 and -17 transcription factors are modulators of the bZIP28 branch of the unfolded protein response during PAMP-triggered immunity in Arabidopsis thaliana". Plant Science. DOI: 10.1016/j.plantsci.2018.09.019".

Henríquez-Valencia, C; Arenas-M, A; Medina, J; Canales, J. 2018. "Integrative transcriptomic analysis uncovers novel gene modules that underlie the sulfate response in Arabidopsis thaliana". Frontiers in Plant Science. DOI: 10.3389/fpls.2018.00470".

Perez-Alonso, MM; Carrasco-Loba, V; Medina, J; Vicente-Carbajosa, J; Pollmann, S. 2018. "When transcriptomics and metabolomics work hand in hand: A case study characterizing plant CDF transcription factors". High Throughput. DOI: 10.3390/ht7010007".

Gras, DE; Vidal, EA; Undurraga, SF; Riveras, E; Moreno, S; Dominguez-Figueroa, J; Alabadi, D; Blázquez, M; Medina, J; Gutiérrez, RA. 2017. "SMZ/SNZ and gibberellin signaling are required for nitrate-elicited delay of flowering time in Arabidopsis thaliana". Journal of Experimental Botany. DOI: 10.1093/jxb/erx423".

Renau-Morata, B; Molina, RV; Carrillo, L; Cebolla-Cornejo, J; Sánchez-Perales, M; Pollmann, S; Dominguez-Figueroa, J; Corrales, AR; Flexas, J; Vicente-Carbajosa, J; MEDINA, J; Nebauer, S. 2017. "Ectopic expression of CDF3 genes in tomato enhances biomass production and yield under salinity stress conditions". Frontiers in Plant Science. DOI: 10.3389/fpls.2017.00660".

Corrales, A-R; Carrillo, L; Lasierra, P; Nebauer, SG; Dominguez-Figueroa, J; Renau-Morata, B; Pollmann, S; Granell, A; Molina, R-V; Vicente-Carbajosa, J; Medina, J. 2017. "Multifaceted role of Cycling Dof Factor 3 (CDF3) in the regulation of flowering time and abiotic stress responses in Arabidopsis". Plant, Cell & Environment. DOI: 10.1111/pce.12894".

Hossain, A; Henríquez-Valencia, C; Gómez-Páez, M; Medina, J; Orellana, A; Vicente-Carbajosa, J; Zouhar, J. 2016. "Identification of novel components of the Unfolded Protein Response in Arabidopsis". Frontiers in Plant Science. DOI: 10.3389/fpls.2016.00650".

Corrales, A-R; Nebauer, SG; Carrillo, L; Fernández-Nohales, P; Marqués, J; Renau-Morata, B; Granell, A; Pollmann, S; Vicente-Carbajosa, J; Molina, R-V; Medina, J. 2014. "Characterization of tomato Cycling Dof Factors reveals conserved and new functions in the control of flowering time and abiotic stress responses". Journal of Experimental Botany. DOI: 10.1093/jxb/ert451".

Zanin, M; Medina Alcazar, J; Vicente Carbajosa, J; Gomez Paez, M; Papo, D; Sousa, P; Menasalvas, E; Boccaletti, S. 2014. "Parenclitic networks: uncovering new functions in biological data". Scientific Reports. DOI: 10.1038/srep05112".

Corrales, R; Carrillo, L; Nebauer, SG; Renau-Morata, B; Sánchez-Perales, M; Fernández-Nohales, P; Marqués, J; Granell, A; Pollmann, S; Vicente-Carbajosa, J; Molina, RV; Medina, J. 2014. "Salinity assay in Arabidopsis". Bio-protocol. DOI:

Renau-Morata, B; Sánchez-Perales, M; Medina, J; Molina, RV; Corrales, R; Carrillo, L; Fernández-Nohales, P; Marqués, J; Pollmann, S; Vicente-Carbajosa, J; Granell, A; Nebauer, SG. 2014. "Salinity assay in tomato". Bio-protocol. DOI:

Hentrich, M; Bottcher, C; Duchting, P; Cheng, Y; Zhao, Y; Berkowitz, O; Masle, J; Medina, J; Pollmann, S. 2013. "The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression". Plant Journal. DOI: 10.1111/tpj.12152".

Hentrich, M; Sánchez-Parra, B; Pérez Alonso, M-M; Carrasco Loba, V; Carrillo, L; Vicente-Carbajosa, J; Medina, J; Pollmann, S. 2013. "YUCCA8 and YUCCA9 overexpression reveals a link between auxin signaling and lignification through the induction of ethylene biosynthesis". Plant Signaling & Behavior. DOI: 10.4161/psb.26363".