METAL HOMEOSTASIS IN PLANT-MICROBE INTERACTIONS

Group leader: Manuel González-Guerrero - Professor
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Lab Web Page: http://metalsym.com

 

Personnel:

 

 

Plant-microbe interactions are influenced by essential transition metal nutrients (iron, copper, zinc...)

 

Iron, copper, zinc, and some other transition metals are essential nutrients for life, but they are scarce. Prevalent low metal availability in many of the main agricultural areas of the world reduce crop production and nutritional value, and this is worsened by climate change. However, metal metabolism is a double-edge sword, since slightly higher levels of metals are also poisonous for most life forms. Our group is dedicated to studying the molecular bases of the exquisite balance that maintains transition metal homeostasis and how this is impacted by beneficial and prejudicial plant-microbe interactions. To do this, we use classical genetic and biochemical approaches, with state-of-the-art metal imaging approaches.

 

Global zinc deficiency distribution (left, Alloway, 2008). Distribution of metal-contaminated soils in Europe (right, Tóth et al., 2016)

 

 

Research objectives


1.- Transition metal exchange in beneficial plant-microbe interactions. Two of the best studied beneficial plant-microbe interactions are arbuscular mycorrhizal fungi (AMF) and rhizobia. AMF colonize over 80% of terrestrial plants providing essential nutrients to the host. We are studying how AMF deliver key transition metals and how the host plant accepts them, in an analogous mechanism to what has been reported for phosphate. In contrast to AMF, rhizobia are mostly restricted to legumes, where they colonize specialized root organs, the nodules. Within the nodules, rhizobia differentiate into nitrogen-fixing symbiosomes, a process that is heavily reliant on transition metals. We are characterizing the transporters responsible for metal allocation for symbiotic nitrogen fixation and determining how it is controlled.


Left Zinc transporter MtZIP6 (red) localization in Medicago truncatula nodule cells. Rhizobia are shown in green and nuclei in blue (Abreu et al., 2017) Right: Iron (green), calcium (red), and zinc (blue) distribution in M. Truncatula nodules (Rodríguez-Haas et al., 2013).

 


2.- Specific cytosolic transition metal allocation. Transition metals are never free, hydrated, in the cytosol, but bound to a plethora of simple molecules and proteins. Consequently, from a few plasma membrane transporters, metals are specifically targeted to hundreds of apo-metalloproteins, in a process likely mediated by metallochaperones. Very little or nothing is known about iron, zinc, or molybdenum-chaperones in plants or bacteria, and plant copper-chaperone have been largely overlooked. We are identifying and analyzing new metallochaperones, particularly in the context of biological nitrogen fixation, a process with a large demand for these elements.


Proposed copper exchange pathway in M. truncatula nodule cells. MT indicates protein fron the host plant and Sm proteins fron teh associated rhizobium Sinorhizobium meliloti. PM indicates plasma membrane; SM, symbiosome membrane; OM, rhizobial outer membrane ; and IM, rhizobial inner membrane. Obtained from Senovilla at el., 2018.)

 

 

3.- Transition metal homeostasis in plant-pathogen interactions. Transition metals are essential at low levels and toxic at slightly higher ones. Modulating their local availability is used as a strategy to fend-off invading microbes in animals and plants. We are focused on unveiling the molecular bases of metal-based innate immunity in plants and in improving these pathways in crops.



Growth of Pseudomonas aeruginosa WT, simple and double mutants in Cu+-ATPases CopA1 and CopA2, and complemented lines in Arabidopsis thaliana leaves. Adapted from González-Guerrero et al., 2010.)

 

 

Funding

  1. Role of copper in plant innate immunity (2020-2023). Comunidad de Madrid (IND2019/BIO-17117). PI Manuel González-Guerrero
  2. Role of plant Cu+-chaperones in intracellular copper trafficking in symbiotic nitrogen fixation (2019-2021). Agencia Estatal de Investigación (PGC2018-095996-B). PI Manuel González-Guerrero
  3. Diverting metals to Medicago truncatula nodules (2016-2018). Plan Estatal MINECO (AGL-2015-65866-P). PI Manuel González-Guerrero.
  4. Metal Transport in the Tripartite Symbiosis Arbuscular Mycorrhizal Fungi-Legume-Rhizobia (2014-2019). European Research Council Starting Grant. PI: Manuel González-Guerrero
  5. Transporte de metales al nódulo de Medicago truncatula (2013-2015). Plan Nacional MINECO (AGL-2012-32974). PI: Manuel González-Guerrero.
  6. Metal homeostasis in nodulated Medicago plants (2011-2015). Marie Curie International Reintegration Grant (PIRG8-GA-2010-276771). PI: Manuel González-Guerrero.

 


Publications in the last five years (full list here)

De, A., Hoang, C.V., Escudero, V., Armas, A.M., Echavarri-Erasun, C., González-Guerrero, M., Jordá, L. 2024. Combating plant diseases through transition metal allocation. New Phytologist. DOI: 10.1111/nph.20366

Barahona, E., Collantes-García, J.A., Rosa-Núñez, E., Xiong, J., Jiang, X., Jiménez-Vicente, E., Echávarri-Erasun, C., Guo, Y., Rubio, L.M., González-Guerrero, M. 2024. Azotobacter vinelandii scaffold protein NifU transfers iron to NifQ as part of the iron-molybdenum cofactor biosynthesis pathway for nitrogenase. Journal of Biological Chemistry 107900. DOI: 10.1016/j.jbc.2024.107900

Lin, J., Bjørk, P.K., Kolte, M.V., Poulsen, E., Dedic, E., Drace, T., Andersen, S.U., Nadzieja, M., Liu, H., Castillo-Michel, H., Escudero, V., González-Guerrero, M., Boesen, T., Pedersen, J.S., Stougaard, J., Andersen, K.R., Reid, D. 2024. Zinc mediates control of nitrogen fixation via transcription factor filamentation. Nature 1–6. DOI: 10.1038/s41586-024-07607-6

Escudero, V., Fuenzalida, M., Rezende, E.L., González-Guerrero, M., Roschzttardtz, H. 2024. Perspectives on embryo maturation and seed quality in a global climate change scenario. Journal of Experimental Botany erae154. DOI: 10.1093/jxb/erae154

Fuenzalida, M., Gómez, M.I., Ferrada, E., Díaz, C., Escudero, V., González-Guerrero, M., Jordana, X., Roschzttardtz, H. 2023. Using an embryo specific promoter to modify iron distribution pattern in Arabidopsis. Plant Science 111931. DOI: 10.1016/j.plantsci.2023.111931

Rosa-Núñez, E., Echavarri-Erasun, C., Armas, A.M., Escudero, V., Poza-Carrión, C., Rubio, L.M., González-Guerrero, M. 2023. Iron Homeostasis in Azotobacter vinelandii. Biology 12, 1423. DOI: 10.3390/biology12111423

Navarro-Gómez, C., León-Mediavilla, J., Küpper, H., Rodríguez-Simón, M., Paganelli-López, A., Wen, J., Burén, S., Mysore, K.S., Bokhari, S.N.H., Imperial, J., Escudero, V., González-Guerrero, M. 2023. Nodule-specific Cu+-chaperone NCC1 is required for symbiotic nitrogen fixation in Medicago truncatula root nodules. New Phytologist. DOI: 10.1111/nph.19360

González-Guerrero, M., Navarro-Gómez, C., Rosa-Núñez, E., Echávarri-Erasun, C., Imperial, J., Escudero, V. 2023. Forging a symbiosis: transition metal delivery in symbiotic nitrogen fixation. New Phytologist. DOI: 10.1111/nph.19098

Mihelj, P., Abreu, I., Moreyra, T., González-Guerrero, M., Raimunda, D. 2023. Functional Characterization of the Co2+ Transporter AitP in Sinorhizobium meliloti: A New Player in Fe2+ Homeostasis. Applied and Environmental Microbiology e01901-22. DOI: 10.1128/aem.01901-22

Assunção, A.G.L., Cakmak, I., Clemens, S., González-Guerrero, M., Nawrocki, A., Thomine, S. 2022. Micronutrient homeostasis in plants for more sustainable agriculture and healthier human nutrition. Journal of Experimental Botany erac014. DOI: 10.1093/jxb/erac014

Escudero, V., Ferreira Sánchez, D., Abreu, I., Sopeña-Torres, S., Makarovsky-Saavedra, N., Bernal, M., Krämer, U., Grolimund, D., González-Guerrero, M., Jordá, L. 2022. Arabidopsis thaliana Zn 2+-efflux ATPases HMA2 and HMA4 are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina BMM. Journal of Experimental Botany. DOI: 10.1093/jxb/erab400

Castro-Rodríguez, R., Escudero, V., Reguera, M., Gil-Díez, P., Quintana, J., Prieto, R.I., Kumar, R.K., Brear, E., Grillet, L., Wen, J., Mysore, K.S., Walker, E.L., Smith, P.M.C., Imperial, J., González-Guerrero, M. 2021. Medicago truncatula Yellow Stripe-Like7 encodes a peptide transporter participating in symbiotic nitrogen fixation. Plant, Cell & Environment. DOI: 10.1111/pce.14059

Gavrin, A., Loughlin, P.C., Brear, E., Griffith, O.W., Bedon, F., Suter Grotemeyer, M., Escudero, V., Reguera, M., Qu, Y., Mohd-Noor, S.N., Chen, C., Borges Osorio, M., Rentsch, D., González-Guerrero, M., Day, D.A., Smith, P.M.C. 2021. Soybean Yellow Stripe-like 7 is a symbiosome membrane peptide transporter important for nitrogen fixation. Plant Physiology. DOI: 10.1093/plphys/kiab044

Senovilla, M., Abreu, I., Escudero, V., Cano, C., Bago, A., Imperial, J., González-Guerrero, M. 2020. MtCOPT2 is a Cu+ transporter specifically expressed in Medicago truncatula mycorrhizal roots. Mycorrhiza. DOI: 10.1007/s00572-020-00987-3

Castro-Rodríguez, R., Abreu, I., Reguera, M., Novoa-Aponte, L., Mijovilovich, A., Escudero, V., Jiménez-Pastor, F.J., Abadía, J., Wen, J., Mysore, K.S., Álvarez-Fernández, A., Küpper, H., Imperial, J., González-Guerrero, M. 2020. Medicago truncatula Yellow Stripe1-Like3 gene is involved in vascular delivery of transition metals to root nodules. Journal of Experimental Botany. DOI: 10.1093/jxb/eraa390

Orr, R.G., Foley, S.J., Sherman, C.A., Abreu, I., Galotto, G., Liu, B., Gonzalez-Guerrero, M., Vidali, L. 2020. Robust survival-based RNAi of gene families using in tandem silencing of adenine phosphoribosyltransferase. Plant Physiology. DOI: 10.1104/pp.20.00865

Escudero, V., Abreu, I., Tejada‐Jiménez, M., Rosa‐Núñez, E., Quintana, J., Prieto, R.I., Larue, C., Wen, J., Villanova, J., Mysore, K.S., Argüello, J.M., Castillo‐Michel, H., Imperial, J., González‐Guerrero, M. 2020. Medicago truncatula Ferroportin2 mediates iron import into nodule symbiosomes. New Phytologist. DOI: 10.1111/nph.16642

Galotto, G., Abreu, I., Sherman, C.A., Liu, B., Gonzalez-Guerrero, M., Vidali, L. 2020. Chitin Triggers Calcium-mediated Immune Response in the Plant Model Physcomitrella patens. Molecular Plant-Microbe Interactions®. DOI: 10.1094/MPMI-03-20-0064-R

Escudero, V., Abreu, I., del Sastre, E., Tejada-Jiménez, M., Larue, C., Novoa-Aponte, L., Castillo-González, J., Wen, J., Mysore, K.S., Abadía, J., Argüello, J.M., Castillo-Michel, H., Álvarez-Fernández, A., Imperial, J., González-Guerrero, M. 2020. Nicotianamine Synthase 2 Is Required for Symbiotic Nitrogen Fixation in Medicago truncatula Nodules. Frontiers in Plant Science 10, 1780. DOI: 10.3389/fpls.2019.01780

Abreu, I., Escudero, V., Montiel, J., Castro‐Rodríguez, R., González-Guerrero, M. 2019. Metal transport in Medicago truncatula nodule rhizobia-infected cells, in: The Model Legume Medicago Truncatula. John Wiley & Sons, Ltd, pp. 652–664. DOI: 10.1002/9781119409144.ch81

Roschzttardtz, H., González-Guerrero, M., Gomez-Casati, D.F. 2019. Editorial: Metallic Micronutrient Homeostasis in Plants. Frontiers in Plant Science 10, 927. DOI: 10.3389/fpls.2019.00927

Ibeas, M.A., Grant-Grant, S., Coronas, M.F., Vargas-Pérez, J.I., Navarro, N., Abreu, I., Castillo-Michel, H., Avalos-Cembrano, N., Paez Valencia, J., Perez, F., González-Guerrero, M., Roschzttardtz, H. 2019. The Diverse Iron Distribution in Eudicotyledoneae Seeds: From Arabidopsis to Quinoa. Frontiers in Plant Science 9, 1985. DOI: 10.3389/fpls.2018.01985