Rodríguez Egea, Pedro Luís
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- PublicationStructure-Based Modulation of the Ligand Sensitivity of a Tomato Dimeric Abscisic Acid Receptor Through a Glu to Asp Mutation in the Latch Loop(Frontiers Media SA, 2022-06-06) Infantes, Lourdes; Rivera-Moreno, Maria; Daniel-Mozo, Miguel; Benavente, Juan Luis; Ocaña-Cuesta, Javier; Coego, Alberto; Lozano Juste, Jorge; Rodríguez Egea, Pedro Luís; Albert, Armando; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Agencia Estatal de Investigación; Ministerio de Ciencia e Innovación[EN] The binding of the plant phytohormone Abscisic acid (ABA) to the family of ABA receptors (PYR/PYL/RCAR) triggers plant responses to abiotic stress. Thus, the implementation of genetic or chemical strategies to modulate PYR/PYL activity might be biotechnologically relevant. We have employed the available structural information on the PYR/PYL receptors to design SlPYL1, a tomato receptor, harboring a single point mutation that displays enhanced ABA dependent and independent activity. Interestingly, crystallographic studies show that this mutation is not directly involved in ABA recognition or in the downstream phosphatase (PP2C) inhibitory interaction, rather, molecular dynamic based ensemble refinement restrained by crystallographic data indicates that it enhances the conformational variability required for receptor activation and it is involved in the stabilization of an active form of the receptor. Moreover, structural studies on this receptor have led to the identification of niacin as an ABA antagonist molecule in vivo. We have found that niacin blocks the ABA binding site by mimicking ABA receptor interactions, and the niacin interaction inhibits the biochemical activity of the receptor.
- PublicationThe fungal sesquiterpenoid pyrenophoric acid B uses the plant ABA biosynthetic pathway to inhibit seed germination(Oxford University Press, 2019-10-01) Lozano Juste, Jorge; Masi, Marco; Cimmino, Alessio; Clement, Suzette; FERNÁNDEZ LÓPEZ, MARIA ANGELES; Antoni, Regina; Meyer, Susan; Rodríguez Egea, Pedro Luís; Evidente, Antonio; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; European Commission; Compagnia di San Paolo; U.S. Department of Agriculture; U.S. Department of the Interior; Ministerio de Educación, Cultura y Deporte; Università degli Studi di Napoli Federico II; Ministerio de Ciencia, Innovación y Universidades; Agencia Estatal de Investigación[EN] Pyrenophoric acid (P-Acid), P-Acid B, and P-Acid C are three phytotoxic sesquiterpenoids produced by the ascomycete seed pathogen Pyrenophora semeniperda, a fungus proposed as a mycoherbicide for biocontrol of cheatgrass, an extremely invasive weed. When tested in cheatgrass bioassays, these metabolites were able to delay seed germination, with P-Acid B being the most active compound. Here, we have investigated the cross-kingdom activity of P-Acid B and its mode of action, and found that it activates the abscisic acid (ABA) signaling pathway in order to inhibit seedling establishment. P-Acid B inhibits seedling establishment in wild-type Arabidopsis thaliana, while several mutants affected in the early perception as well as in downstream ABA signaling components were insensitive to the fungal compound. However, in spite of structural similarities between ABA and P-Acid B, the latter is not able to activate the PYR/PYL family of ABA receptors. Instead, we have found that P-Acid B uses the ABA biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to reduce seedling establishment. We propose that the fungus P. semeniperda manipulates plant ABA biosynthesis as a strategy to reduce seed germination, increasing its ability to cause seed mortality and thereby increase its fitness through higher reproductive success.
- PublicationPYL8 ABA receptors of Phoenix dactylifera play a crucial role in response to abiotic stress and are stabilized by ABA.(Oxford University Press, 2021-02-02) García-Maquilón, Irene; Coego, Alberto; Lozano Juste, Jorge; Messerer, Maxim; de Ollas, Carlos; Julian, Jose; Ruiz Partida, Rafael; Pizzio, Gaston; Belda Palazón, Borja; Gómez-Cadenas, Aurelio; Mayer, Klaus F. X.; Geiger, Dietmar; Alquraishi, Saleh A.; Alrefaei, Abdulwahed F.; Ache, Peter; Hedrich, Rainer; Rodríguez Egea, Pedro Luís; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas[EN] The identification of those prevalent abscisic acid (ABA) receptors and molecular mechanisms that trigger drought adaptation in crops well adapted to harsh conditions such as date palm (Phoenix dactylifera, Pd) sheds light on plant-environment interactions. We reveal that PdPYL8-like receptors are predominantly expressed under abiotic stress, with Pd27 being the most expressed receptor in date palm. Therefore, subfamily I PdPYL8-like receptors have been selected for ABA signaling during abiotic stress response in this crop. Biochemical characterization of PdPYL8-like and PdPYL1-like receptors revealed receptor- and ABA-dependent inhibition of PP2Cs, which triggers activation of the pRD29B-LUC reporter in response to ABA. PdPYLs efficiently abolish PP2C-mediated repression of ABA signaling, but loss of the Trp lock in the seed-specific AHG1-like phosphatase PdPP2C79 markedly impairs its inhibition by ABA receptors. Characterization of Arabidopsis transgenic plants that express PdPYLs shows enhanced ABA signaling in seed, root, and guard cells. Specifically, Pd27-overexpressing plants showed lower ABA content and were more efficient than the wild type in lowering transpiration at negative soil water potential, leading to enhanced drought tolerance. Finally, PdPYL8-like receptors accumulate after ABA treatment, which suggests that ABA-induced stabilization of these receptors operates in date palm for efficient boosting of ABA signaling in response to abiotic stress.
- PublicationRBR-type E3 ligases and the Ub-conjugating enzyme UBC26 regulate ABA receptor levels and signaling(American Society of Plant Biologists, 2020-04) FERNÁNDEZ LÓPEZ, MARIA ANGELES; Belda Palazón, Borja; Julian, J.; Coego Gonzalez, Alberto; Lozano Juste, Jorge; Iñigo, Sabrina; RODRIGUEZ, LESIA; Bueso Ródenas, Eduardo; Goossens, Alain; Rodríguez Egea, Pedro Luís; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Departamento de Biotecnología; Escuela Técnica Superior de Ingeniería Agronómica y del Medio Natural; European Commission; Generalitat Valenciana; European Regional Development Fund; Belgian Federal Science Policy Office; Ministerio de Educación, Cultura y Deporte; Consejo Superior de Investigaciones Científicas; Agencia Estatal de Investigación; Ministerio de Economía y Competitividad[EN] The turnover of abscisic acid (ABA) signaling core components modulates the plant's response to ABA and is regulated by ubiquitination. We show that Arabidopsis (Arabidopsis thaliana) RING Finger ABA-Related1 (RFA1) and RFA4 E3 ubiquitin ligases, members of the RING between RING fingers (RBR)-type RSL1/RFA family, are key regulators of ABA receptor stability in root and leaf tissues, targeting ABA receptors for degradation in different subcellular locations. RFA1 is localized both in the nucleus and cytosol, whereas RFA4 shows specific nuclear localization and promotes nuclear degradation of ABA receptors. Therefore, members of the RSL1/RFA family interact with ABA receptors at plasma membrane, cytosol, and nucleus, targeting them for degradation via the endosomal/vacuolar RSL1-dependent pathway or 26S proteasome. Additionally, we provide insight into the physiological function of the relatively unexplored plant RBR-type E3 ligases, and through mutagenesis and biochemical assays we identified cysteine-361 in RFA4 as the putative active site cysteine, which is a distinctive feature of RBR-type E3 ligases. Endogenous levels of PYR1 and PYL4 ABA receptors were higher in the rfa1 rfa4 double mutant than in wild-type plants. UBC26 was identified as the cognate nuclear E2 enzyme that interacts with the RFA4 E3 ligase and forms UBC26-RFA4-receptor complexes in nuclear speckles. Loss-of-function ubc26 alleles and the rfa1 rfa4 double mutant showed enhanced sensitivity to ABA and accumulation of ABA receptors compared with the wild type. Together, our results reveal a sophisticated mechanism by which ABA receptors are targeted by ubiquitin at different subcellular locations, in which the complexity of the ABA receptor family is mirrored in the partner RBR-type E3 ligases.
- PublicationStructure of Ligand-Bound Intermediates of Crop ABA Receptors Highlights PP2C as Necessary ABA Co-receptor(Elsevier, 2017) Moreno-Alvero, María; Yunta, C.; González Guzmán, Miguel; Lozano Juste, Jorge; Benavente, J.L.; Arbona, V.; Menendez, M; Martínez Ripoll, Martín; Infantes, L.; Gómez-Cadenas, Aurelio; Rodríguez Egea, Pedro Luís; Albert, A.; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Economía y Competitividad; European Commission
- PublicationInactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants(American Association for the Advancement of Science, 2015-09-01) Castillo López del Toro, Mª Cruz; Lozano Juste, Jorge; González Guzmán, Miguel; Rodriguez, Lesia; Rodríguez Egea, Pedro Luís; Leon Ramos, Jose; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Ciencia e Innovación[EN] Abscisic acid (ABA) is a phytohormone that inhibits growth and enhances adaptation to stress in plants. ABA perception and signaling rely on its binding to receptors of the pyrabactin resistance1/PYR1-like/regulatory components of ABA receptors (PYR/PYL/RCAR) family, the subsequent inhibition of clade A type 2C protein phosphatases (PP2Cs), and the phosphorylation of ion channels and transcription factors by protein kinases of the SnRK2 family. Nitric oxide (NO) may inhibit ABA signaling because NO-deficient plants are hypersensitive to ABA. Regulation by NO often involves posttranslational modification of proteins. Mass spectrometry analysis of ABA receptors expressed in plants and recombinant receptors modified in vitro revealed that the receptors were nitrated at tyrosine residues and S-nitrosylated at cysteine residues. In an in vitro ABA-induced, PP2C inhibition assay, tyrosine nitration reduced receptor activity, whereas S-nitrosylated receptors were fully capable of ABA-induced inhibition of the phosphatase. PYR/PYL/RCAR proteins with nitrated tyrosine, which is an irreversible covalent modification, were poly-ubiquitylated and underwent proteasome-mediated degradation. We propose that tyrosine nitration, which requires NO and superoxide anions, is a rapid mechanism by which NO limits ABA signaling under conditions in which NO and reactive oxygen species are both produced.
- PublicationThe MATH-BTB BPM3 and BPM5 subunits of Cullin3-RING E3 ubiquitin ligases target PP2CA and other clade A PP2Cs for degradation(Proceedings of the National Academy of Sciences, 2019-07-30) Julian-Valenzuela, Jose; Coego Gonzalez, Alberto; Lozano Juste, Jorge; Lechner, Esther; Wu, Qian; Zhang, Xu; Merilo, Ebe; Belda Palazón, Borja; Park, Sang-Youl; Cutler, Sean R.; An, Chengcai; Genschik, Pascal; Rodríguez Egea, Pedro Luís; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; European Commission; Generalitat Valenciana; Estonian Research Council; European Regional Development Fund; Agence Nationale de la Recherche, Francia; Consejo Superior de Investigaciones Científicas; Agencia Estatal de Investigación; Ministerio de Economía y Competitividad[EN] Early abscisic acid signaling involves degradation of clade A protein phosphatases type 2C (PP2Cs) as a complementary mechanism to PYR/PYL/RCAR-mediated inhibition of PP2C activity. At later steps, ABA induces up-regulation of PP2C transcripts and protein levels as a negative feedback mechanism. Therefore, resetting of ABA signaling also requires PP2C degradation to avoid excessive ABA-induced accumulation of PP2Cs. It has been demonstrated that ABA induces the degradation of existing ABI1 and PP2CA through the PUB12/13 and RGLG1/5 E3 ligases, respectively. However, other unidentified E3 ligases are predicted to regulate protein stability of clade A PP2Cs as well. In this work, we identified BTB/POZ AND MATH DOMAIN proteins (BPMs), substrate adaptors of the multimeric cullin3 (CUL3)-RING-based E3 ligases (CRL3s), as PP2CA-interacting proteins. BPM3 and BPM5 interact in the nucleus with PP2CA as well as with ABI1, ABI2, and HAB1. BPM3 and BPM5 accelerate the turnover of PP2Cs in an ABA-dependent manner and their overexpression leads to enhanced ABA sensitivity, whereas bpm3 bpm5 plants show increased accumulation of PP2CA, ABI1 and HAB1, which leads to global diminished ABA sensitivity. Using biochemical and genetic assays, we demonstrated that ubiquitination of PP2CA depends on BPM function. Given the formation of receptor-ABA-phosphatase ternary complexes is markedly affected by the abundance of protein components and ABA concentration, we reveal that BPMs and multimeric CRL3 E3 ligases are important modulators of PP2C coreceptor levels to regulate early ABA signaling as well as the later desensitizing-resetting steps.
- PublicationPre-mRNA splicing repression triggers abiotic stress signaling in plants(Blackwell Publishing, 2017) Ling, Yu; Alshareef, Sahar; Butt, Haroon; Lozano Juste, Jorge; Li, Lixin; Galal, Aya A.; Moustafa, Ahmed; Momin, Afaque A.; Tashkandi, Manal; Richardson, Dale N.; Fujii, Hiroaki; Arold, Stefan; Rodríguez Egea, Pedro Luís; Duque, Paula; Mahfouz, Magdy M.; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Economía y Competitividad[EN] Alternative splicing (AS) of precursor RNAs enhances transcriptome plasticity and proteome diversity in response to diverse growth and stress cues. Recent work has shown that AS is pervasive across plant species, with more than 60% of intron-containing genes producing different isoforms. Mammalian cell-based assays have discovered various inhibitors of AS. Here, we show that the macrolide pladienolide B (PB) inhibits constitutive splicing and AS in plants. Also, our RNA sequencing (RNA-seq) data revealed that PB mimics abiotic stress signals including salt, drought and abscisic acid (ABA). PB activates the abiotic stress-and ABA-responsive reporters RD29A::LUC and MAPKKK18::uidA in Arabidopsis thaliana and mimics the effects of ABA on stomatal aperture. Genome-wide analysis of AS by RNA-seq revealed that PB perturbs the splicing machinery and leads to a striking increase in intron retention and a reduction in other forms of AS. Interestingly, PB treatment activates the ABA signaling pathway by inhibiting the splicing of clade A PP2C phosphatases while still maintaining to some extent the splicing of ABA-activated SnRK2 kinases. Taken together, our data establish PB as an inhibitor and modulator of splicing and a mimic of abiotic stress signals in plants. Thus, PB reveals the molecular underpinnings of the interplay between stress responses, ABA signaling and post-transcriptional regulation in plants.
- PublicationUnnatural agrochemical ligands for engineered abscisic acid receptors(Elsevier (Cell Press), 2015-06) Rodríguez Egea, Pedro Luís; Lozano Juste, Jorge; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas[EN] Existing agrochemicals can be endowed with new applications through protein engineering of plant receptors. A recent study shows an engineered PYR1 ABA receptor can be activated by mandipropamid. Plants engineered with such PYR1 variant are responsive to this agrochemical, which confers protection against drought through activation of ABA signaling.
- PublicationAbscisic acid mimic-fluorine derivative 4 alleviates water deficit stress by regulating ABA-responsive genes, proline accumulation, CO2 assimilation, water use efficiency and better nutrient uptake in tomato plants(Frontiers Media SA, 2023-06-08) Jimenez-Arias, David; Morales-Sierra, Sarai; Suárez, Emma; Lozano Juste, Jorge; Coego, Alberto; Estevez, Juan C.; Borges, Andrés A.; Rodríguez Egea, Pedro Luís; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Xunta de Galicia; Generalitat Valenciana; Ministerio de Ciencia e Innovación[EN] Water deficit represents a serious limitation for agriculture and both genetic and chemical approaches are being used to cope with this stress and maintain plant yield. Next-generation agrochemicals that control stomatal aperture are promising for controlling water use efficiency. For example, chemical control of abscisic acid (ABA) signaling through ABA-receptor agonists is a powerful method to activate plant adaptation to water deficit. Such agonists are molecules able to bind and activate ABA receptors and, although their development has experienced significant advances in the last decade, few translational studies have been performed in crops. Here, we describe protection by the ABA mimic-fluorine derivative 4 (AMF4) agonist of the vegetative growth in tomato plants subjected to water restriction. Photosynthesis in mock-treated plants is markedly impaired under water deficit conditions, whereas AMF4 treatment notably improves CO2 assimilation, the relative plant water content and growth. As expected for an antitranspirant molecule, AMF4 treatment diminishes stomatal conductance and transpiration in the first phase of the experiment; however, when photosynthesis declines in mock-treated plants as stress persists, higher photosynthetic and transpiration parameters are recorded in agonist-treated plants. Additionally, AMF4 increases proline levels over those achieved in mock-treated plants in response to water deficit. Thus water deficit and AMF4 cooperate to upregulate P5CS1 through both ABA-independent and ABA-dependent pathways, and therefore, higher proline levels are produced Finally, analysis of macronutrients reveals higher levels of Ca, K and Mg in AMF4- compared to mock-treated plants subjected to water deficit. Overall, these physiological analyses reveal a protective effect of AMF4 over photosynthesis under water deficit and enhanced water use efficiency after agonist treatment. In summary, AMF4 treatment is a promising approach for farmers to protect the vegetative growth of tomatoes under water deficit stress.