ROOT SYSTEM DEVELOPMENT DURING THE INTERACTION OF PLANTS WITH SOIL MICROORGANISMS


Group leader: Javier Cabrera Chaves - Ramón y Cajal fellow
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Personnel:

 

 

Introduction


Our research seeks to respond to the imperative need to find solutions to the adverse conditions (abiotic stresses) that crops are suffering and will suffer to a greater extent in the future, due to climate change. The study of the architecture of the plant root system has always been of vital importance to agriculture. Roots anchor plants to the soil and allow them to reach dispersed water and nutrients, alleviating abiotic stresses to which they are subjected such as drought, salinity or nutritional deficits. This would justify the extensive and successful research carried out in recent decades on the molecular pathways governing root and lateral root development, mainly in the model plant Arabidopsis thaliana. In addition to the growth of the primary root, the root system expands by the formation of lateral roots. By increasing the number of lateral roots, plants increase the exchangeable area of the root system with the soil and improve their anchorage and resilience. There are different control points during lateral root formation such as the auxin maximum in the oscillation zone, the formation of pre-branching sites or the first divisions of the founder cells.


In the current scenario where high temperatures, periods of floods and droughts, as well as decreasing biodiversity and humidity are major effects of the climate crisis on soils, the implementation of this knowledge to improve the root system architecture of crops is of vital importance. However, the extensive knowledge gained in vitro with model plants is often confronted with difficulties in its implementation in field-grown plants. The use of rhizosphere microorganisms as biological amendments is increasing because of the need to improve plant productivity due to the increasingly frequent pesticide ban, the warning about overuse of fertilisers and the immediate scenario of drought and flooding periods accompanying the climatic emergency. Many studies have described the ability of rhizosphere microorganisms to promote plant and root system growth, known as plant growth-promoting microorganisms. Among them, rhizobacteria have been the most studied. However, although the beneficial effect of non-pathogenic fungi, such as endophytes, on root development and stress relief is known, molecular studies on how they interfere with developmental programmes are scarcer. It is important to understand which genes and processes are involved in increasing lateral root formation during the interaction.


The use of root endophytic fungi as biological manipulators to understand lateral root development could bring novel information to the field: do endophytes alleviate abiotic stresses by increasing the root system, do endophytes sequester molecular pathways to increase the number of lateral roots equal to or different from those already described, do these fungi have effector molecules that directly alter or induce these pathways, or is it only an indirect response from the plant? Answering these questions may represent that new and known molecular pathways leading to lateral root formation in Arabidopsis could be more easily manipulated in crop plants by using endophytes as biological switches.


Objectives of the research line


The main objective of this line would be to understand how fungi in the rhizosphere could alleviate the stresses generated by climate change by favouring the formation of lateral roots. To know if they alter the frequency and/or intensity of expression changes in the root oscillation zone, and/or modify the number of pre-branch sites and founder cells, with the future perspective of obtaining healthier, more productive and resilient crops.

In the short term we are pursuing the following objectives:

- To find plant-fungus interactions that modify the number and/or density of lateral roots under stress and control conditions. We will test the ability of collections of endophytic fungi to produce changes in the number of lateral roots in plants subjected to abiotic stresses and control conditions.



- To elucidate the molecular pathways responsible for enhancing lateral root formation during biotic interactions. To obtain the transcriptome by RNAseq, as well as the hormone profile, of different plant tissues inoculated with selected fungi with an effect on the oscillation zone and/or the number of pre-branch sites and/or lateral roots. In this way, candidate genes, gene pathways or altered physiological mechanisms, which facilitate increased stress resistance with increased number of lateral roots, will be monitored and validated using different approaches, such as evaluation of phenotypes in mutants for members of the identified pathways, observation of fluorescent marker lines of members of these pathways, quantitative PCR, etc.

- To find fungal isolates with a positive effect on crop resilience in soil. One of the main threats associated with climate change is water stress and soil salinity resulting from high atmospheric temperatures. The selected fungi in the interaction with Arabidopsis will be tested under more realistic conditions resulting from climate change (under different stresses on greenhouse grown plants).

 

Funding


  1. Elucidating the molecular mechanisms enhancing lateral root formation during the interaction between plants and endophytic fungi. PID2022-141938OA-I00. 01/09/2023- Agencia Estatal Investigación. PI: Dr. Cabrera. 181.250 €.
  2. Deciphering the cell and molecular cues underlying plant-biotic interactions to reprogram the root system. RYC2021-030913-I. 01/01/2023-. Agencia Estatal Investigación. PI: Dr. Cabrera. 45000 €.

 


Representative Publications

Perez-Garcia, P., Pucciariello, O., Sanchez-Corrionero, A., Cabrera, J., del Barrio, C., del Pozo, J.C., Perales, M., Wabnik, K., Moreno-Risueno, M.A. 2023. The cold-induced factor CBF3 mediates root stem cell activity, regeneration, and developmental responses to cold. Plant Communications, Focus Issue on Climate Change and Food Security: Plant Science Roles 4, 100737. DOI: 10.1016/j.xplc.2023.100737


Cabrera, J., Conesa, C.M., del Pozo, J.C. 2022. May the dark be with roots: a perspective on how root illumination may bias in vitro research on plant–environment interactions. New Phytologist 233, 1988–1997. DOI: 10.1111/nph.17936


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 sequencing reveals order of tissue initiation. Molecular Plant 14, 1362–1378. 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


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., Pernas, M., 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 227, 200–215. DOI: 10.1111/nph.16521


Olmo, R., Cabrera, J., Moreno-Risueno, M.A., 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 8. DOI: 10.3389/fpls.2017.00875


Cabrera, J., Barcala, M., García, A., Rio-Machín, A., Medina, C., Jaubert-Possamai, S., Favery, B., Maizel, A., Ruiz-Ferrer, V., Fenoll, C., Escobar, C. 2016. Differentially expressed small RNAs in Arabidopsis galls formed by Meloidogyne javanica: a functional role for miR390 and its TAS3-derived tasiRNAs. New Phytologist 209, 1625–1640. DOI: 10.1111/nph.13735


Cabrera, J., Díaz-Manzano, F.E., Sanchez, M., Rosso, M.-N., Melillo, T., Goh, T., Fukaki, H., Cabello, S., Hofmann, J., Fenoll, C., Escobar, C. 2014. A role for LATERAL ORGAN BOUNDARIES-DOMAIN 16 during the interaction Arabidopsis–Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development. New Phytologist 203, 632–645. DOI: 10.1111/nph.12826