SIGNALING NETWORKS IN PLANT RESPONSES TO NITROGEN AND SULPHUR LIMITATION

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


Twitter @medinajoaquin1

Background

In nature, plants usually grow in soil that contains very low amounts of macronutrients like Nitrogen and Sulphur or conditions with an unbalanced proportion of both macronutrients. To adapt and grow in nutrient-deprived environments, plants have developed sophisticated strategies and molecular mechanisms. Notably, plant nutrient stress responses also integrate other environmental inputs such as light, temperature and water to optimize nutrient uptake, metabolism and growth.

 

Our research group is focused on the effects of nutrition limitation in plant development. We are specifically interested in how N/S limitation impacts primary metabolism and that modulates root and fruit growth and development. These are key elements to understand the plasticity of plant organogenesis but also important factors to improve nutrient use efficiency, biomass production and the quality of fruits /seeds, which are central problems in sustainable agriculture.

 

To achieve these objectives, we work with the model plant Arabidopsis and crop species such as tomato. We are studying the impact of Nutrient systemic signaling on plant development using various genetic, molecular and systems biology strategies that highlighted new connections between the nutrient signaling and the partition of photo-assimilates and the developmental program of roots and fruits.

 

RESEARCH LINES:

 

Deciphering N systemic signaling and root forage response in plants

Up to now, a few components involved in systemic N signaling have been identified in Arabidopsis, including some peptides, nitrogenous metabolites and several plant hormones. However, very little is known about how plant sense N levels (“N status”), and how this information is integrated in a general reprograming of gene expression. We are studying the regulatory networks involved in N limitation responses, though multiple molecular/metabolomic strategies and analyzing the role of the identified transcription factors (TFs) of the bZIP, DOF, TCP, ARF, NLP and NF-YA5 classes in N local and systemic signaling and root forage response in Arabidopsis. We have identified conserved and novel roles for the identified TFs in the response to N limitation that revealed new connections between systemic signaling and partition photo-assimilates and roots/fruits development.

 

Figure: Root nutrient foraging responses. Expression analysis strategy used to identify new regulatory components in Arabidopsis and tomato.

 


Exploring nutrient regulation of signaling and transcription in Solanaceae

Up to now most of the knowledge and the studies to investigate the impact of N/S limitation in plant growth and development and yield have been conducted in the model plant Arabidopsis. Thus, we are studying the components and signaling pathways involved in N/S sensing and partitioning in other plant species or crops like tomato. In particular, we have conducted different integrative transcriptomic and metabolomic strategies under different Nutrient conditions to dissect the nutrient stress pathways in tomato. Our work highlights the importance of C and N/S metabolism and remobilization and uncovered new key N-regulated genes, including different regulatory factors of the bZIP, DOF, ARF, NLP and NF-YA5 classes, which play key roles in N responses in Arabidopsis.

 

Figure. Integrative analysis of transcriptomic A) and metabolomic (B) data revealed significant correlations between different gene clusters and specific metabolomic compounds (C) involved in responses to N limitation in tomato.

 


Characterization of CDF proteins, new master hubs in plant N/C metabolism, nutrient partition and plant response to stress

The previously described approaches allowed the identification of group of DOF transcription factors, whose transcripts oscillate under constant light conditions named Cycling Dof Factors (CDF1-5); that play additional functions regulating Nitrogen and Carbon metabolism and root growth responses in Arabidopsis. In addition, our data supports that CDFs are potential candidate genes for improving nutrient use efficiency (NUE), N/C partition, and yield in tomato and potato.


Figure. CDF functions in N/C metabolism. A) General scheme of CDF functions in N/C metabolism. B) The overexpression of CDF3 in tomato enhanced NUE, biomass and yield. C) The targeted overexpression of SlCDF4 in the fruit enhances tomato size and yield involving gibberellin signaling.

 

 

 


Dissecting Natural variation in Nutrient stress responses in Solanaceae

To date, most of the crop varieties have been selected, and therefore domesticated, under non-limiting nutrient conditions. Consequently, there has been a significant loss of genetic variation associated with nutrient use efficiency in the actual crop varieties. 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.

 

During the last years, we analyzed the existing natural variation for NUE associated traits in a panel of commercial tomato varieties and wild relatives and identified a set of genotypes with contrasting NUE. Our work highlighted different biological processes and physiological strategies in the regulation of N responses in plants and leads the ways to new strategies to improve NUE in crops. In addition, molecular and physiological analyses of advanced mapping populations between commercial varieties and tomato wild relatives, identified different QTLs associated to plant growth, yield, and fruit quality traits (N-QTLs) as well as candidate genes behind them.


Figure. Analysis of NUE related traits in a panel of commercial tomato varieties and wild relatives and identified under deferent N supply (A-B). Identification of N-QTLs associated to plant growth, yield, and fruit quality traits (C) (N-QTLs) and candidate genes behind them.

 

 

FUNDING:

  1. 2023-2025. ROOTS FOR THE FUTURE: know-how and biotechnological applications to improve productivity and resilience under stress conditions. -RED2022-134836-T. Agencia Estatal de Investigación.
  2. 2022-2026- PLANTG_01_SUPERGREENFACTORIES: Missions-CBGP:  MISSIONS-CBGP- SEVERO OCHOA (SO-CBGP) (EoI-MCBGP21).
  3. 2022-2025 PLANTG_05_ROOTCLOCK: MISSIONS-CBGP-SEVERO OCHOA (SO-CBGP) (EoI-MCBGP21).
  4. 2021-2023. NUETOM. (PID2020- 114165RR-C21). Molecular analyses of Nitrogen responses in tomato genotypes with contrasting NUE. Agencia Estatal de Investigación PI Joaquin Medina.
  5. 2019-2023. VEG-ADAPT. EU PRIMA (PCI2019-103610 –EU). “Adapting Mediterranean vegetable crops to climate change-induced multiple stresses”. PI Joaquin Medina.
  6. 2018-2020. SO-CBGP-EoI2017. CBGP 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.
  7. 2017-2020. (CA15138 COST) “TRANSAUTOPHAGY: European Network of Multidisciplinary Research and Translation of Autophagy knowledge.
  8. 2017-2019. REDI170024. CONICYT. “RINAP” Red Iberoamericana de la Nutrición de Azufre en Plantas”. PIs Joaquín Medina, Javier Canales.
  9. 2017-2020. R-00014-C02-00. Improvement of tomato production through increased carbon assimilation and nitrogen use efficiency using transcription regulators. Agencia Estatal de Investigación. PI Joaquín Medina

 


Representative Publications

Renau-Morata, B., Jiménez-Benavente, E., Gil-Villar, D., Cebolla-Cornejo, J., Romero-Hernández, G., Carrillo, L., Vicente-Carbajosa, J., Medina, J., Molina, R.V., Nebauer, S.G. 2024. Arabidopsis CDF3 transcription factor increases carbon and nitrogen assimilation and yield in trans-grafted tomato plants. Plant Physiology and Biochemistry 210, 108607. DOI: 10.1016/j.plaphy.2024.108607

Renau-Morata, B., Cebolla-Cornejo, J., Carrillo, L., Gil-Villar, D., Martí, R., Jiménez-Gómez, J.M., Granell, A., Monforte, A.J., Medina, J., Molina, R.V., Nebauer, S.G. 2024. Identification of Solanum pimpinellifolium genome regions for increased resilience to nitrogen deficiency in cultivated tomato. Scientia Horticulturae 323, 112497. DOI: 10.1016/j.scienta.2023.112497

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".