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1. Synthetically derived BiAux modulates auxin co-receptor activity to stimulate lateral root formation

Author

Ministerio de Ciencia y Tecnología (España), Agencia Estatal de Investigación (España), European Commission, González-García, Mary Paz [0000-0002-3739-3368], Saez, Angela [0000-0002-9189-4737], Lanza, Mónica [0009-0002-5868-9296], Hoyos, Pilar [0000-0001-6053-2437], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Pacios, Luis F. [0000-0002-0585-4289], Gradillas, Ana [0000-0001-7290-5210], Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Hernaiz, María José [0000-0003-3897-1104], Pozo, Juan Carlos del [0000-0002-4113-457X], González-García, Mary Paz, Saez, Angela, Lanza, Mónica, Hoyos, Pilar, Bustillo-Avendaño, Estefano, Pacios, Luis F., Gradillas, Ana, Moreno-Risueño, Miguel Ángel, Hernaiz, María José, Pozo, Juan Carlos del, Ministerio de Ciencia y Tecnología (España), Agencia Estatal de Investigación (España), European Commission, González-García, Mary Paz [0000-0002-3739-3368], Saez, Angela [0000-0002-9189-4737], Lanza, Mónica [0009-0002-5868-9296], Hoyos, Pilar [0000-0001-6053-2437], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Pacios, Luis F. [0000-0002-0585-4289], Gradillas, Ana [0000-0001-7290-5210], Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Hernaiz, María José [0000-0003-3897-1104], Pozo, Juan Carlos del [0000-0002-4113-457X], González-García, Mary Paz, Saez, Angela, Lanza, Mónica, Hoyos, Pilar, Bustillo-Avendaño, Estefano, Pacios, Luis F., Gradillas, Ana, Moreno-Risueño, Miguel Ángel, Hernaiz, María José, and Pozo, Juan Carlos del

Abstract

The root system plays an essential role in plant growth and adaptation to the surrounding environment. The root clock periodically specifies lateral root prebranch sites (PBS), where a group of pericycle founder cells (FC) is primed to become lateral root founder cells and eventually give rise to lateral root primordia or lateral roots (LRs). This clock-driven organ formation process is tightly controlled by modulation of auxin content and signaling. Auxin perception entails the physical interaction of TRANSPORT INHIBITOR RESPONSE 1 (TIR1) or AUXIN SIGNALING F-BOX (AFBs) proteins with AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) repressors to form a co-receptor system. Despite the apparent simplicity, the understanding of how specific auxin co-receptors are assembled remains unclear. We identified the compound bis-methyl auxin conjugated with N-glucoside, or BiAux, in Arabidopsis (Arabidopsis thaliana) that specifically induces the formation of PBS and the emergence of LR, with a slight effect on root elongation. Docking analyses indicated that BiAux binds to F-box proteins, and we showed that BiAux function depends on TIR1 and AFB2 F-box proteins and AUXIN RESPONSE FACTOR 7 activity, which is involved in FC specification and LR formation. Finally, using a yeast (Saccharomyces cerevisiae) heterologous expression system, we showed that BiAux favors the assemblage of specific co-receptors subunits involved in LR formation and enhances AUXIN/INDOLE-3-ACETIC ACID 28 protein degradation. These results indicate that BiAux acts as an allosteric modulator of specific auxin co-receptors. Therefore, BiAux exerts a fine-tune regulation of auxin signaling aimed to the specific formation of LR among the many development processes regulated by auxin.

Published
2024

2. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis

Author

Ministerio de Economía y Competitividad (España), European Commission, Comunidad de Madrid, Research Foundation - Flanders, Agencia Estatal de Investigación (España), Ministerio de Ciencia e Innovación (España), Perianez-Rodriguez, Juan [0000-0003-1002-7111], Rodriguez, Marcos [0000-0003-3741-8593], Marconi, Marco [0000-0002-3457-1384], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Wachsman, Guy [0000-0002-0551-9333], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], De Gernier, Hugues [0000-0002-7644-3233], Cabrera, Javier [0000-0002-9277-4876], Perez-Garcia, Pablo [0000-0001-8595-8530], Gude, Inmaculada [0000-0002-3122-1688], Saez, Angela [0000-0002-9189-4737], Serrano-Ron, Laura [0000-0001-5180-6547], Beeckman, Tom [0000-0001-8656-2060], Benfey, Philip N [0000-0001-5302-758X], Rodríguez-Patón, Alfonso [0000-0001-7289-2114], del Pozo, J. C. [0000-0002-4113-457X], Wabnik, Krzysztof [0000-0001-7263-0560], Moreno-Risueno, Miguel A [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, De Gernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, Moreno-Risueño, Miguel Ángel, Ministerio de Economía y Competitividad (España), European Commission, Comunidad de Madrid, Research Foundation - Flanders, Agencia Estatal de Investigación (España), Ministerio de Ciencia e Innovación (España), Perianez-Rodriguez, Juan [0000-0003-1002-7111], Rodriguez, Marcos [0000-0003-3741-8593], Marconi, Marco [0000-0002-3457-1384], Bustillo-Avendaño, Estefano [0000-0002-1442-8791], Wachsman, Guy [0000-0002-0551-9333], Sanchez-Corrionero, Alvaro [0000-0001-5360-0294], De Gernier, Hugues [0000-0002-7644-3233], Cabrera, Javier [0000-0002-9277-4876], Perez-Garcia, Pablo [0000-0001-8595-8530], Gude, Inmaculada [0000-0002-3122-1688], Saez, Angela [0000-0002-9189-4737], Serrano-Ron, Laura [0000-0001-5180-6547], Beeckman, Tom [0000-0001-8656-2060], Benfey, Philip N [0000-0001-5302-758X], Rodríguez-Patón, Alfonso [0000-0001-7289-2114], del Pozo, J. C. [0000-0002-4113-457X], Wabnik, Krzysztof [0000-0001-7263-0560], Moreno-Risueno, Miguel A [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, De Gernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, and Moreno-Risueño, Miguel Ángel

Abstract

In Arabidopsis, the root clock regulates the spacing of lateral organs along the primary root through oscillating gene expression. The core molecular mechanism that drives the root clock periodicity and how it is modified by exogenous cues such as auxin and gravity remain unknown. We identified the key elements of the oscillator (AUXIN RESPONSE FACTOR 7, its auxin-sensitive inhibitor IAA18/POTENT, and auxin) that form a negative regulatory loop circuit in the oscillation zone. Through multilevel computer modeling fitted to experimental data, we explain how gene expression oscillations coordinate with cell division and growth to create the periodic pattern of organ spacing. Furthermore, gravistimulation experiments based on the model predictions show that external auxin stimuli can lead to entrainment of the root clock. Our work demonstrates the mechanism underlying a robust biological clock and how it can respond to external stimuli.

Published
2021

3. Role of cis-zeatin in root responses to phosphate starvation

Author

Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Comunidad de Madrid, Silva-Navas, J. [0000-0003-1567-1184], Conesa, Carlos M. [0000-0002-3113-4576], Saez, Angela [0000-0002-9189-4737], Navarro Neila, Sara [0000-0002-9335-5665], Garcia-Mina, J. M. [0000-0001-6352-9612], Zamarreño, Angel M. [0000-0003-1966-0239], Baigorri, R. [0000-0002-9197-5895], Swarup, Ranjan [0000-0002-6438-9188], del Pozo, J. C. [0000-0002-4113-457X], Silva-Navas, J., Conesa, Carlos M., Saez, Angela, Navarro Neila, Sara, Garcia-Mina, J. M., Zamarreño, Angel M., Baigorri, R., Swarup, Ranjan, del Pozo, J. C., Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Comunidad de Madrid, Silva-Navas, J. [0000-0003-1567-1184], Conesa, Carlos M. [0000-0002-3113-4576], Saez, Angela [0000-0002-9189-4737], Navarro Neila, Sara [0000-0002-9335-5665], Garcia-Mina, J. M. [0000-0001-6352-9612], Zamarreño, Angel M. [0000-0003-1966-0239], Baigorri, R. [0000-0002-9197-5895], Swarup, Ranjan [0000-0002-6438-9188], del Pozo, J. C. [0000-0002-4113-457X], Silva-Navas, J., Conesa, Carlos M., Saez, Angela, Navarro Neila, Sara, Garcia-Mina, J. M., Zamarreño, Angel M., Baigorri, R., Swarup, Ranjan, and del Pozo, J. C.

Abstract

Phosphate (Pi) is an essential nutrient for all organisms. Roots are underground organs, but the majority of the root biology studies have been done on root systems growing in the presence of light. Root illumination alters the Pi starvation response (PSR) at different intensities. Thus, we have analyzed morphological, transcriptional and physiological responses to Pi starvation in dark-grown roots. We have identified new genes and pathways regulated by Pi starvation that were not described previously. We also show that Pi-starved plants increase the cis-zeatin (cZ) : trans-zeatin (tZ) ratio. Transcriptomic analyses show that tZ preferentially represses cell cycle and PSR genes, whereas cZ induces genes involved in cell and root hair elongation and differentiation. In fact, cZ-treated seedlings show longer root system as well as longer root hairs compared with tZ-treated seedlings, increasing the total absorbing surface. Mutants with low cZ concentrations do not allocate free Pi in roots during Pi starvation. We propose that Pi-starved plants increase the cZ : tZ ratio to maintain basal cytokinin responses and allocate Pi in the root system to sustain its growth. Therefore, cZ acts as a PSR hormone that stimulates root and root hair elongation to enlarge the root absorbing surface and to increase Pi concentrations in roots.

Published
2019

4. The polyadenylation factor FIP1 is important for plant development and root responses to abiotic stresses

Author

Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), Téllez-Robledo, B. [0000-0002-0846-9992], Manzano, Concepción [0000-0003-1592-5068], Saez, Angela [0000-0002-9189-4737], Navarro Neila, Sara [0000-0002-9335-5665], Silva-Navas, J. [0000-0002-0938-910X], de Lorenzo, L. [0000-0001-5422-3339], González García, M. Paz [0000-0002-3739-3368], Toribio, René [0000-0002-4847-629X], Hunt, Arthur G. [0000-0002-0008-4158], Baigorri, R. [0000-0002-9197-5895], Casimiro, Ilda [0000-0002-5817-9176], Brady, Siobhan M. [0000-0001-9424-8055], Castellano Moreno, María Mar [0000-0003-0339-4247], del Pozo, J. C. [0000-0002-4113-457X], Téllez-Robledo, B., Manzano, Concepción, Saez, Angela, Navarro Neila, Sara, Silva-Navas, J., de Lorenzo, L., González García, M. Paz, Toribio, René, Hunt, Arthur G., Baigorri, R., Casimiro, Ilda, Brady, Siobhan M., Castellano Moreno, María Mar, del Pozo, J. C., Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), Téllez-Robledo, B. [0000-0002-0846-9992], Manzano, Concepción [0000-0003-1592-5068], Saez, Angela [0000-0002-9189-4737], Navarro Neila, Sara [0000-0002-9335-5665], Silva-Navas, J. [0000-0002-0938-910X], de Lorenzo, L. [0000-0001-5422-3339], González García, M. Paz [0000-0002-3739-3368], Toribio, René [0000-0002-4847-629X], Hunt, Arthur G. [0000-0002-0008-4158], Baigorri, R. [0000-0002-9197-5895], Casimiro, Ilda [0000-0002-5817-9176], Brady, Siobhan M. [0000-0001-9424-8055], Castellano Moreno, María Mar [0000-0003-0339-4247], del Pozo, J. C. [0000-0002-4113-457X], Téllez-Robledo, B., Manzano, Concepción, Saez, Angela, Navarro Neila, Sara, Silva-Navas, J., de Lorenzo, L., González García, M. Paz, Toribio, René, Hunt, Arthur G., Baigorri, R., Casimiro, Ilda, Brady, Siobhan M., Castellano Moreno, María Mar, and del Pozo, J. C.

Abstract

Root development and its response to environmental changes is crucial for whole plant adaptation. These responses include changes in transcript levels. Here, we show that the alternative polyadenylation (APA) of mRNA is important for root development and responses. Mutations in FIP1, a component of polyadenylation machinery, affects plant development, cell division and elongation, and response to different abiotic stresses. Salt treatment increases the amount of poly(A) site usage within the coding region and 5' untranslated regions (5'-UTRs), and the lack of FIP1 activity reduces the poly(A) site usage within these non-canonical sites. Gene ontology analyses of transcripts displaying APA in response to salt show an enrichment in ABA signaling, and in the response to stresses such as salt or cadmium (Cd), among others. Root growth assays show that fip1-2 is more tolerant to salt but is hypersensitive to ABA or Cd. Our data indicate that FIP1-mediated alternative polyadenylation is important for plant development and stress responses.

Published
2019

5. An auxin-regulable oscillatory circuit drives the root clock in Arabidopsis

Author

Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, DeGernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, Moreno-Risueño, Miguel Ángel, Moreno-Risueño, Miguel Ángel [0000-0002-9794-1450], Perianez-Rodriguez, Juan, Rodriguez, Marcos, Marconi, Marco, Bustillo-Avendaño, Estefano, Wachsman, Guy, Sanchez-Corrionero, Alvaro, DeGernier, Hugues, Cabrera, Javier, Pérez-García, Pablo, Gude, Inmaculada, Saez, Angela, Serrano-Ron, Laura, Beeckman, Tom, Benfey, Philip N., Rodríguez-Patón, Alfonso, del Pozo, J. C., Wabnik, Krzysztof, and Moreno-Risueño, Miguel Ángel

Abstract

In Arabidopsis, the root clock regulates the spacing of lateral organs along the primary root through oscillating gene expression. The core molecular mechanism that drives the root clock periodicity and how it is modified by exogenous cues such as auxin and gravity remain unknown. We identified the key elements of the oscillator (AUXIN RESPONSE FACTOR 7, its auxin-sensitive inhibitor IAA18/POTENT, and auxin) that form a negative regulatory loop circuit in the oscillation zone. Through multilevel computer modeling fitted to experimental data, we explain how gene expression oscillations coordinate with cell division and growth to create the periodic pattern of organ spacing. Furthermore, gravistimulation experiments based on the model predictions show that external auxin stimuli can lead to entrainment of the root clock. Our work demonstrates the mechanism underlying a robust biological clock and how it can respond to external stimuli.

Published
2021

6. Alternative Polyadenylation and Salicylic Acid Modulate Root Responses to Low Nitrogen Availability

Author

Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), Conesa, Carlos M. [0000-0002-3113-4576], Navarro Neila, Sara [0000-0002-9335-5665], de Lorenzo, L. [0000-0001-5422-3339], Hunt, Arthur G. [0000-0002-0008-4158], Baigorri, R. [0000-0002-9197-5895], Garcia-Mina, J. M. [0000-0001-6352-9612], Zamarreño, Angel M. [0000-0003-1966-0239], Sacristán, Soledad [0000-0002-5753-2644], del Pozo, J. C. [0000-0002-4113-457X], Conesa, Carlos M., Saez, Angela, Navarro Neila, Sara, de Lorenzo, L., Hunt, Arthur G., Sepúlveda, Edgar B., Baigorri, R., Garcia-Mina, J. M., Zamarreño, Angel M., Sacristán, Soledad, del Pozo, J. C., Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), Conesa, Carlos M. [0000-0002-3113-4576], Navarro Neila, Sara [0000-0002-9335-5665], de Lorenzo, L. [0000-0001-5422-3339], Hunt, Arthur G. [0000-0002-0008-4158], Baigorri, R. [0000-0002-9197-5895], Garcia-Mina, J. M. [0000-0001-6352-9612], Zamarreño, Angel M. [0000-0003-1966-0239], Sacristán, Soledad [0000-0002-5753-2644], del Pozo, J. C. [0000-0002-4113-457X], Conesa, Carlos M., Saez, Angela, Navarro Neila, Sara, de Lorenzo, L., Hunt, Arthur G., Sepúlveda, Edgar B., Baigorri, R., Garcia-Mina, J. M., Zamarreño, Angel M., Sacristán, Soledad, and del Pozo, J. C.

Abstract

Nitrogen (N) is probably the most important macronutrient and its scarcity limits plant growth, development and fitness. N starvation response has been largely studied by transcriptomic analyses, but little is known about the role of alternative polyadenylation (APA) in such response. In this work, we show that N starvation modifies poly(A) usage in a large number of transcripts, some of them mediated by FIP1, a component of the polyadenylation machinery. Interestingly, the number of mRNAs isoforms with poly(A) tags located in protein-coding regions or 5'-UTRs significantly increases in response to N starvation. The set of genes affected by APA in response to N deficiency is enriched in N-metabolism, oxidation-reduction processes, response to stresses, and hormone responses, among others. A hormone profile analysis shows that the levels of salicylic acid (SA), a phytohormone that reduces nitrate accumulation and root growth, increase significantly upon N starvation. Meta-analyses of APA-affected and fip1-2-deregulated genes indicate a connection between the nitrogen starvation response and salicylic acid (SA) signaling. Genetic analyses show that SA may be important for preventing the overgrowth of the root system in low N environments. This work provides new insights on how plants interconnect different pathways, such as defense-related hormonal signaling and the regulation of genomic information by APA, to fine-tune the response to low N availability.

Published
2020

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