ROOT ORGANOGENESIS, REGENERATION AND ROOTING

Group leader: Miguel Ángel Moreno Risueño - Assistant Professor
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Personnel:

 

Multicellular organisms are made up of organs that are critical for survival and perform specific functions: reproduction, water and nutrient uptake, photosynthesis, etc. Plant embryos, unlike animal embryos, only contain primary organs. However, most organs at a plant’s adult or reproductive state are newly made after embryogenesis. Thus, in order to complete their life cycle, plants need to develop postembryonic organs for nutrition, anchorage, reproduction, etc.

We use as a model the root of the plant Arabidopsis thaliana. This is an excellent model because we can observe morphogenic processes in vivo. Our goals aim to discover:

How do plants locate new roots at specific positions?
How do plants form new roots from founder cells?
How do plants regenerate root organs after chemical or physical wound?
How do plants root?

How do plants locate new roots at specific positions?

Positioning of organs determines plants’ morphology. We have shown that periodic oscillation of gene expression at the root tip marks the position of new roots (Movie 1). Gene oscillations are part of the Lateral Root Clock (Moreno-Risueno et al., 2010) and require cell reprogramming. In addition, the hormone auxin plays an important role in maintaining gene oscillations. The genetic and molecular bases of cell selection and reprogramming remain largely unexplored. We have identified gene mutants with altered positioning of postembryonic roots (Figure 1). We are currently studying the interaction of these genes with the Lateral Root Clock and auxin signaling.

 

 

How do plants form new roots from founder cells?

Cells are reprogrammed to form root founder cells. Root founder cells divide following certain rules and organizing principles to form new organs. An unexplored key aspect of this process is how new tissues and cell types are formed and arranged following specific patterns. We are studying the first divisions of root founder cells. Our goal is to discover what types of cells are formed and the morphogenetic underlying mechanism. Part of our research involves marking certain cells in vivo with fluorescent markers, isolating those cells and studying their developmental programs (Figure 2).
 


 

How do plants regenerate root organs after wound?

Plants have amazing regeneration capabilities. Chemo-toxic treatment can kill many meristematic cells of roots, but still roots are able to regenerate (Figure 3). We are studying how roots form new tissues after chemo-toxic treatment as part of their regenerative mechanism. This research investigates the role of certain factors in establishing cell lineages that will generate new tissues from stem cells.

How do plants root?

Green parts of plants are able to root. Leaves can grow new roots in hormone-free medium (Figure 4). We are investigating the role of auxin signaling and cell-type specific factors in forming a new root from leaves. Our goal is to determine if there are common developmental mechanisms shared with other morphogenic developmental processes.



Funding

REGULATORY MECHANISMS AND SIGNALING MOLECULES DURING POSTEMBRYONIC ROOT FORMATION. Ministerio de Ciencia e Innovación. Programa estatal de fomento de la investigación científica y técnica de excelencia. Proyectos I+D+i - Modalidades “Retos Investigación” y “Generación de Conocimiento”. Proyecto PID2019-111523GB-I00 financiado por MCIN/ AEI /10.13039/501100011033. 

NEW MECHANISMS SPECIFYING AND REGENERATING POSTEMBRYONIC ORGANS IN THE ARABIDOPSIS ROOT. Ministry of Economy and Competitiveness –MINECO- Programa estatal de fomento de la investigación científica y técnica de excelencia. BFU2016-80315-P. 2017-2019.

IDENTIFICATION AND CHARACTERIZATION OF THE DETERMINATION CUES OF ADULT PLANT CELL PLURIPOTENCY USING THE ARABIDOPSIS ROOT. Ministry of Economy and Competitiveness –MINECO- Programa estatal de fomento de la investigación científica y técnica de excelencia. BFU2013-41160-P. 2014-2017. Fondo Europeo de Desarrollo Regional (FEDER).

A MOLECULAR, GENOMICS AND GENETIC ANALYSIS OF NEW STEM CELL FORMATION DURING ROOT MORPHOGENESIS. FP7-PEOPLE-2012-CIG- 322082-Curie Integration Grant. UE. 2012-2016.

SPECIFICATION OF NEW STEM CELLS IN THE ARABIDOPSIS THALIANA ROOT. Ministry of Science and Innovation –MICINN- Programa Ramon y Cajal. RYC-2011-09049. 2012-2017.

 
 


Representative Publications

Abril-Urias, P., Ruiz-Ferrer, V., Cabrera, J., Olmo, R., Silva, A.C., Díaz-Manzano, F.E., Domínguez-Figueroa, J., Martínez-Gómez, Á., Gómez-Rojas, A., Moreno-Risueno, M.Á., Fenoll, C., Escobar, C. 2023. Divergent regulation of auxin responsive genes in root-knot and cyst nematodes feeding sites formed in Arabidopsis. Frontiers in Plant Science 14. DOI: 10.3389/fpls.2023.1024815

Serrano-Ron, L., Cabrera, J., Perez-Garcia, P., Moreno-Risueno, M.A. 2021. Unraveling Root Development Through Single-Cell Omics and Reconstruction of Gene Regulatory Networks. Frontiers in Plant Science 12, 671. DOI: 10.3389/fpls.2021.661361

Serrano-Ron, L., Perez-Garcia, P., Sanchez-Corrionero, A., Gude, I., Cabrera, J., Ip, P.-L., Birnbaum, K.D., Moreno-Risueno, M.A. 2021. RECONSTRUCTION OF LATERAL ROOT FORMATION THROUGH SINGLE-CELL RNA-SEQ REVEALS ORDER OF TISSUE INITIATION. Molecular Plant. DOI: 10.1016/j.molp.2021.05.028

Perianez-Rodriguez, J., Rodriguez, M., Marconi, M., Bustillo-Avendaño, E., Wachsman, G., Sanchez-Corrionero, A., De Gernier, H., Cabrera, J., Perez-Garcia, P., Gude, I., Saez, A., Serrano-Ron, L., Beeckman, T., Benfey, P.N., Rodríguez-Patón, A., del Pozo, J.C., Wabnik, K., Moreno-Risueno, M.A. 2021. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis. Science Advances 7, eabd4722. DOI: 10.1126/sciadv.abd4722

Wachsman, G., Zhang, J., Moreno-Risueno, M.A., Anderson, C.T., Benfey, P.N. 2020. Cell wall remodeling and vesicle trafficking mediate the root clock in Arabidopsis. Science 370, 819–823. DOI: 10.1126/science.abb7250

Clark, N.M., Fisher, A.P., Berckmans, B., Broeck, L.V. den, Nelson, E.C., Nguyen, T.T., Bustillo-Avendaño, E., Zebell, S.G., Moreno-Risueno, M.A., Simon, R., Gallagher, K.L., Sozzani, R. 2020. Protein complex stoichiometry and expression dynamics of transcription factors modulate stem cell division. Proceedings of the National Academy of Sciences 117, 15332–15342. DOI: 10.1073/pnas.2002166117

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González-García, M.-P., Bustillo-Avendaño, E., Sanchez-Corrionero, A., del Pozo, J.C., Moreno-Risueno, M.A. 2020. Fluorescence-Activated Cell Sorting Using the D-Root Device and Optimization for Scarce and/or Non-Accessible Root Cell Populations. Plants 9, 499. DOI: 10.3390/plants9040499

Olmo, R., Cabrera, J., Díaz‐Manzano, F.E., Ruiz‐Ferrer, V., Barcala, M., Ishida, T., García, A., Andrés, M.F., Ruiz‐Lara, S., Verdugo, I., Ochoa, M.P., Fukaki, H., del Pozo, J.C., Moreno‐Risueno, M.Á., Kyndt, T., Gheysen, G., Fenoll, C., Sawa, S., Escobar, C. 2020. Root-knot nematodes induce gall formation by recruiting developmental pathways of post-embryonic organogenesis and regeneration to promote transient pluripotency. New Phytologist. DOI: 10.1111/nph.16521

Bustillo-Avendaño, E; Ibáñez, S; Sanz, O; Sousa Barros, JA; Gude, I; Perianez-Rodriguez, J; Micol, JL; Del Pozo, JC; Moreno-Risueno, MA; Pérez-Pérez, JM. 2018. "Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis". Plant Physiology. DOI: 10.1104/pp.17.00980".

Manzano, C; Pallero-Baena, M; Silva-Navas, J; Navarro Neila, S; Casimiro, I; Casero, P; Garcia-Mina, JM; Baigorri, R; Rubio, L; Fernandez, JA; Norris, M; Ding, Y; Moreno-Risueno, MA; del Pozo, JC. 2017. "A light-sensitive mutation in Arabidopsis LEW3 reveals the important role of N-glycosylation in root growth and development". Journal of Experimental Botany. DOI: 10.1093/jxb/erx324".

Olmo, R; Cabrera, J; Moreno-Risueno, MA; Fukaki, H; Fenoll, C; Escobar, C. 2017. "Molecular transducers from roots are triggered in Arabidopsis leaves by root-knot nematodes for successful feeding site formation: A conserved post-embryogenic de novo organogenesis program?". Frontiers in Plant Science. DOI: 10.3389/fpls.2017.00875".

Ramirez-Parra, E; Perianez-Rodriguez, J; Navarro-Neila, S; Gude, I; Moreno-Risueno, MA; del Pozo, JC. 2016. "The transcription factor OBP4 controls root growth and promotes callus formation". New Phytologist. DOI: 10.1111/nph.14315".

Silva-Navas, J; Moreno-Risueño, MA; Manzano, C; Téllez-Robledo, B; Navarro-Neila, S; Carrasco, V; Pollmann, S; Gallego, FJ; del Pozo, JC. 2016. "Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition". Plant Cell. DOI: 10.1105/tpc.15.00857".

Moreno-Risueno, MA; Sozzani, R; Yardımcı, GG; Petricka, JJ; Vernoux, T; Blilou, I; Alonso, J; Winter, CM; Ohler, U; Scheres, B; Benfey, PN. 2015. "Transcriptional control of tissue formation throughout root development". Science. DOI: 10.1126/science.aad1171".

Moreno-Risueno, MA; Sozzani, R; Yardımcı, GG; Petricka, JJ; Vernoux, T; Blilou, I; Alonso, J; Winter, CM; Ohler, U; Scheres, B; Benfey, PN. 2015. "Transcriptional control of tissue formation throughout root development". Science. DOI: 10.1126/science.aad1171".

Liberman, LM; Sparks, EE; Moreno-Risueno, MA; Petricka, JJ; Benfey, PN. 2015. "MYB36 regulates the transition from proliferation to differentiation in the Arabidopsis root". Proceedings of the National Academy of Sciences. DOI: 10.1073/pnas.1515576112".

Silva-Navas, J; Moreno-Risueno, MA; Manzano, C; Pallero-Baena, M; Navarro-Neila, S; Téllez-Robledo, B; Garcia-Mina, JM; Baigorri, R; Javier Gallego, F; del Pozo, JC. 2015. "D-Root: a system to cultivate plants with the root in darkness or under different light conditions". Plant Journal. DOI: 10.1111/tpj.12998".

Perianez-Rodriguez, J; Manzano, C; Moreno-Risueno, MA. 2014. "Postembryonic organogenesis and plant regeneration from tissues: two sides of the same coin?". Frontiers in Plant Science. DOI: 10.3389/fpls.2014.00219".