Rodríguez Egea, Pedro Luís
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- PublicationESCRT-I Component VPS23A Affects ABA Signaling by Recognizing ABA Receptors for Endosomal Degradation(Oxford University Press (OUP), 2016-12-05) Yu, Feifei; Lou, Lijuan; Tian, Miaomiao; Li, Qingliang; Ding, Yanglin; Cao, Xiaoqiang; Wu, Yaorong; Belda Palazón, Borja; Rodríguez Egea, Pedro Luís; Yang, Shuhua; Xie, Qi; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; National Key Research and Development Program of China; National Natural Science Foundation of China[EN] Recent discovery of PYR/PYL/RCAR-type abscisic acid (ABA) receptors has become one of most significant advances in plant science in the past decade. In mammals, endosomal sorting acts as an important pathway to downregulate different types of receptors, but its role in plant hormone signaling is poorly understood. Here, we report that an ubiquitin E2-like protein, VPS23A, which is a key component of ESCRT-I, negatively regulates ABA signaling. VPS23A has epistatic relationship with PYR/PYL/RCAR-type ABA receptors and disruption of VPS23A enhanced the activity of key kinase OST1 in the ABA signaling pathway under ABA treatment. Moreover, VPS23A interacts with PYR1/PYLs and K63-linked diubiquitin, and PYL4 possesses K63-linked ubiquitinated modification in vivo. Further analysis revealed that VPS23A affects the subcellular localization of PYR1 and the stability of PYL4. Taken together, our results suggest that VPS23A affects PYR1/PYL4 via vacuole-mediated degradation, providing an advanced understanding of both the turnover of ABA receptors and ESCRTs in plant hormone signaling.
- PublicationTargeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis(American Society of Plant Biologists, 2014-02) Irigoyen, María Luisa; Iniesto, Elisa; Rodríguez Solovey, Leisa Natacha; Puga, Maria Isabel; Yanagawa, Yuki; Pick, Elah; Strickland, Elizabeth; Paz-Ares, Javier; Wei, Ning; De Jaeger, Geert; Rodríguez Egea, Pedro Luís; Deng, Xing Wang; Rubio, Vicente; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Economía y Competitividad; National Science Foundation, EEUU; National Institutes of Health, EEUU[EN] CULLIN4-RING E3 ubiquitin ligases (CRL4s) regulate key developmental and stress responses in eukaryotes. Studies in both animals and plants have led to the identification of many CRL4 targets as well as specific regulatory mechanisms that modulate their function. The latter involve COP10-DET1-DDB1 (CDD)-related complexes, which have been proposed to facilitate target recognition by CRL4, although the molecular basis for this activity remains largely unknown. Here, we provide evidence that Arabidopsis thaliana DET1-, DDB1-ASSOCIATED1 (DDA1), as part of the CDD complex, provides substrate specificity for CRL4 by interacting with ubiquitination targets. Thus, we show that DDA1 binds to the abscisic acid (ABA) receptor PYL8, as well as PYL4 and PYL9, in vivo and facilitates its proteasomal degradation. Accordingly, we found that DDA1 negatively regulates ABA-mediated developmental responses, including inhibition of seed germination, seedling establishment, and root growth. All other CDD components displayed a similar regulatory function, although they did not directly interact with PYL8. Interestingly, DDA1-mediated destabilization of PYL8 is counteracted by ABA, which protects PYL8 by limiting its polyubiquitination. Altogether, our data establish a function for DDA1 as a substrate receptor for CRL4-CDD complexes and uncover a mechanism for the desensitization of ABA signaling based on the regulation of ABA receptor stability.
- PublicationJasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco(National Academy of Sciences, 2011-04-05) Lackman, Petri; González Guzmán, Miguel; Tilleman, Sofie; Carqueijeiro, Ines; Perez Cuellar, Amparo; Moses, Tessa; Seo, Mitsunori; Kanno, Yuri; Hakkinen, Suvi T; Van Montagu, Marc C. E; Thevelein, Johan; Maaheimo, Hannu; Oksman-Caldentey, Kirsi-Marja; Rodríguez Egea, Pedro Luís; Rischer, Heiko; Goossens, Alain; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; European Commission; Ministerio de Ciencia e Innovación[EN] The phytohormones jasmonates (JAs) constitute an important class of elicitors for many plant secondary metabolic pathways. However, JAs do not act independently but operate in complex networks with crosstalk to several other phytohormonal signaling pathways. Here, crosstalk was detected between the JA and abscisic acid (ABA) signaling pathways in the regulation of tobacco (Nicotiana tabacum) alkaloid biosynthesis. A tobacco gene from the PYR/PYL/RCAR family, NtPYL4, the expression of which is regulated by JAs, was found to encode a functional ABA receptor. NtPYL4 inhibited the type-2C protein phosphatases known to be key negative regulators of ABA signaling in an ABA-dependent manner. Overexpression of NtPYL4 in tobacco hairy roots caused a reprogramming of the cellular metabolism that resulted in a decreased alkaloid accumulation and conferred ABA sensitivity to the production of alkaloids. In contrast, the alkaloid biosynthetic pathway was not responsive to ABA in control tobacco roots. Functional analysis of the Arabidopsis (Arabidopsis thaliana) homologs of NtPYL4, PYL4 and PYL5, indicated that also in Arabidopsis altered PYL expression affected the JA response, both in terms of biomass and anthocyanin production. These findings define a connection between a component of the core ABA signaling pathway and the JA responses and contribute to the understanding of the role of JAs in balancing tradeoffs between growth and defense.
- PublicationPlant roots use a patterning mechanism to position lateral root branches toward available water(National Academy of Sciences, 2014-06-24) Bao, Yun; Aggarwal, Pooja; Robbins, Neil E. II; Sturrock, Craig J.; Thompson, Mark C.; Tan, Han Qi; Tham, Cliff; Duan, Lina; Rodríguez Egea, Pedro Luís; Vernoux, Teva; Mooney, Sacha J.; Bennet, Malcolm J.; Dinneny, Jose R.; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Carnegie Institution; National Research Foundation, Singapur; National Science Foundation, EEUU; European Commission; Biotechnology and Biological Sciences Research Council, Reino Unido[EN] The architecture of the branched root system of plants is a major determinant of vigor. Water availability is known to impact root physiology and growth; however, the spatial scale at which this stimulus influences root architecture is poorly understood. Here we reveal that differences in the availability of water across the circumferential axis of the root create spatial cues that determine the position of lateral root branches. We show that roots of several plant species can distinguish between a wet surface and air environments and that this also impacts the patterning of root hairs, anthocyanins, and aerenchyma in a phenomenon we describe as hydropatterning. This environmental response is distinct from a touch response and requires available water to induce lateral roots along a contacted surface. X-ray microscale computed tomography and 3D reconstruction of soil-grown root systems demonstrate that such responses also occur under physiologically relevant conditions. Using early-stage lateral root markers, we show that hydropatterning acts before the initiation stage and likely determines the circumferential position at which lateral root founder cells are specified. Hydro-patterning is independent of endogenous abscisic acid signaling, distinguishing it from a classic water-stress response. Higher water availability induces the biosynthesis and transport of the lateral root-inductive signal auxin through local regulation of TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 and PIN-FORMED 3, both of which are necessary for normal hydropatterning. Our work suggests that water availability is sensed and interpreted at the suborgan level and locally patterns a wide variety of developmental processes in the root.
- 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.
- PublicationRoot hydrotropism is controlled via a cortex-specific growth mechanism(Nature Publishing Group, 2017-06) Dietrich, Daniela; Pang, Lei; Kobayashi, Akie; Fozard, John A.; Boudolf, Veronique; Bhosale, Rahul; Nguyen, Tuan; Hiratsuka, Sotaro; Fujii, Nobuharu; Miyazawa, Yutaka; Bae, Tae-Woong; Wells, Darren M.; Owen, Markus R.; Band, Leah R.; Dyson, Rosemary J.; Rodríguez Egea, Pedro Luís; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Belgian Federal Science Policy Office; Research Foundation Flanders; Ministry of Education, Culture, Sports, Science and Technology, Japón[EN] Plants can acclimate by using tropisms to link the direction of growth to environmental conditions. Hydrotropism allows roots to forage for water, a process known to depend on abscisic acid (ABA) but whose molecular and cellular basis remains unclear. Here we show that hydrotropism still occurs in roots after laser ablation removed the meristem and root cap. Additionally, targeted expression studies reveal that hydrotropism depends on the ABA signalling kinase SnRK2.2 and the hydrotropism-specific MIZ1, both acting specifically in elongation zone cortical cells. Conversely, hydrotropism, but not gravitropism, is inhibited by preventing differential cell-length increases in the cortex, but not in other cell types. We conclude that root tropic responses to gravity and water are driven by distinct tissue-based mechanisms. In addition, unlike its role in root gravitropism, the elongation zone performs a dual function during a hydrotropic response, both sensing a water potential gradient and subsequently undergoing differential growth.
- PublicationThe PYL4 A194T mutant uncovers a key role of PYL4-PP2CA interaction for ABA signaling and plant drought resistance(American Society of Plant Biologists, 2013-09) Pizzio Bianchi, Gaston Alfredo; Rodriguez, Lesia; Antoni-Alandes, Regina; González Guzmán, Miguel; Yunta, Cristina; Merilo, Ebe; Kollist, Hannes; Albert, Armando; Rodríguez Egea, Pedro Luís; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas[EN] Because abscisic acid (ABA) is recognized as the critical hormonal regulator of plant stress physiology, elucidating its signaling pathway has raised promise for application in agriculture, for instance through genetic engineering of ABA receptors. PYRABACTIN RESISTANCE1/PYR1-LIKE (PYL)/REGULATORY COMPONENTS OF ABA RECEPTORS ABA receptors interact with high affinity and inhibit clade A phosphatases type-2C (PP2Cs) in an ABA-dependent manner. We generated an allele library composed of 10,000 mutant clones of Arabidopsis (Arabidopsis thaliana) PYL4 and selected mutations that promoted ABA-independent interaction with PP2CA/ABA-HYPERSENSITIVE3. In vitro protein-protein interaction assays and size exclusion chromatography confirmed that PYL4(A194T) was able to form stable complexes with PP2CA in the absence of ABA, in contrast to PYL4. This interaction did not lead to significant inhibition of PP2CA in the absence of ABA; however, it improved ABA-dependent inhibition of PP2CA. As a result, 35S: PYL4(A194T) plants showed enhanced sensitivity to ABA-mediated inhibition of germination and seedling establishment compared with 35S:PYL4 plants. Additionally, at basal endogenous ABA levels, whole-rosette gas exchange measurements revealed reduced stomatal conductance and enhanced water use efficiency compared with nontransformed or 35S:PYL4 plants and partial up-regulation of two ABA-responsive genes. Finally, 35S:PYL4(A194T) plants showed enhanced drought and dehydration resistance compared with nontransformed or 35S:PYL4 plants. Thus, we describe a novel approach to enhance plant drought resistance through allele library generation and engineering of a PYL4 mutation that enhances interaction with PP2CA.
- PublicationDepletion of abscisic acid levels in roots of flooded Carrizo citrange (Poncirus trifoliata L. Raf. x Citrus sinensis L. Osb.) plants is a stress-specific response associated to the differential expression of PYR/PYL/RCAR receptors(Springer-Verlag, 2017) Arbona, V.; Zandalinas, Sara I.; Manzi, M.; González Guzmán, Miguel; Rodríguez Egea, Pedro Luís; Gómez-Cadenas, Aurelio; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Economía y Competitividad; Universitat Jaume I[EN] Soil flooding reduces root abscisic acid (ABA) levels in citrus, conversely to what happens under drought. Despite this reduction, microarray analyses suggested the existence of a residual ABA signaling in roots of flooded Carrizo citrange seedlings. The comparison of ABA metabolism and signaling in roots of flooded and water stressed plants of Carrizo citrange revealed that the hormone depletion was linked to the upregulation of CsAOG, involved in ABA glycosyl ester (ABAGE) synthesis, and to a moderate induction of catabolism (CsCYP707A, an ABA 8'-hydroxylase) and buildup of dehydrophaseic acid (DPA). Drought strongly induced both ABA biosynthesis and catabolism (CsNCED1, 9-cis-neoxanthin epoxycarotenoid dioxygenase 1, and CsCYP707A) rendering a significant hormone accumulation. In roots of flooded plants, restoration of control ABA levels after stress release was associated to the upregulation of CsBGLU18 (an ABA beta-glycosidase) that cleaves ABAGE. Transcriptional profile of ABA receptor genes revealed a different induction in response to soil flooding (CsPYL5) or drought (CsPYL8). These two receptor genes along with CsPYL1 were cloned and expressed in a heterologous system. Recombinant CsPYL5 inhibited Delta NHAB1 activity in vitro at lower ABA concentrations than CsPYL8 or CsPYL1, suggesting its better performance under soil flooding conditions. Both stress conditions induced ABA-responsive genes CsABI5 and CsDREB2A similarly, suggesting the occurrence of ABA signaling in roots of flooded citrus seedlings. The impact of reduced ABA levels in flooded roots on CsPYL5 expression along with its higher hormone affinity reinforce the role of this ABA receptor under soil-flooding conditions and explain the expression of certain ABA-responsive genes.
- PublicationThe IBO germination quantitative trait locus encodes a phosphatase 2C-related variant with a nonsynonymous amino acid change that interferes with abscisic acid signaling(Wiley, 2015-02) Amiguet-Vercher, Amelia; Santuari, Luca; González Guzmán, Miguel; Depuydt, Stephen; Rodríguez Egea, Pedro Luís; Hardtke, Christian S.; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas[EN] Natural genetic variation is crucial for adaptability of plants to different environments. Seed dormancy prevents precocious germination in unsuitable conditions and is an adaptation to a major macro-environmental parameter, the seasonal variation in temperature and day length. Here we report the isolation of IBO, a quantitative trait locus (QTL) that governs c. 30% of germination rate variance in an Arabidopsis recombinant inbred line (RIL) population derived from the parental accessions Eilenburg-0 (Eil-0) and Loch Ness-0 (Lc-0).IBO encodes an uncharacterized phosphatase 2C-related protein, but neither the Eil-0 nor the Lc-0 variant, which differ in a single amino acid, have any appreciable phosphatase activity in in vitro assays. However, we found that the amino acid change in the Lc-0 variant of the IBO protein confers reduced germination rate. Moreover, unlike the Eil-0 variant of the protein, the Lc-0 variant can interfere with the activity of the phosphatase 2C ABSCISIC ACID INSENSITIVE 1 in vitro. This suggests that the Lc-0 variant possibly interferes with abscisic acid signaling, a notion that is supported by physiological assays. Thus, we isolated an example of a QTL allele with a nonsynonymous amino acid change that might mediate local adaptation of seed germination timing.
- PublicationPYR/RCAR receptors contribute to Ozone-, Reduced Air Humidity-, Darkness- and CO2-Induced Stomatal Regulation(American Society of Plant Biologists, 2013-07) Merilo, Ebe; Laanemets, Kristiina; Hu, Honghong; Shaowu, Xue; Jakobson, Liina; Tulva, Ingmar; González Guzmán, Miguel; Rodríguez Egea, Pedro Luís; Schroeder, Julian; Brosche, Mikael; Kollist, Hannes; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Estonian Ministry of Science and Education; European Regional Development Fund; National Science Foundation, EEUU; National Institutes of Health, EEUU; China Scholarship Council; Shanxi Shengmeitan Occupation Technology Education Development Foundation; Shanxi Province Natural Science Foundation; Ministerio de Economía y Competitividad; European Social Fund[EN] Rapid stomatal closure induced by changes in the environment, such as elevation of CO2, reduction of air humidity, darkness, and pulses of the air pollutant ozone (O-3), involves the SLOW ANION CHANNEL1 (SLAC1). SLAC1 is activated by OPEN STOMATA1 (OST1) and Ca2+-dependent protein kinases. OST1 activation is controlled through abscisic acid (ABA)-induced inhibition of type 2 protein phosphatases (PP2C) by PYRABACTIN RESISTANCE/REGULATORY COMPONENTS OF ABA RECEPTOR (PYR/RCAR) receptor proteins. To address the role of signaling through PYR/RCARs for whole-plant steady-state stomatal conductance and stomatal closure induced by environmental factors, we used a set of Arabidopsis (Arabidopsis thaliana) mutants defective in ABA metabolism/signaling. The stomatal conductance values varied severalfold among the studied mutants, indicating that basal ABA signaling through PYR/RCAR receptors plays a fundamental role in controlling whole-plant water loss through stomata. PYR/RCAR-dependent inhibition of PP2Cs was clearly required for rapid stomatal regulation in response to darkness, reduced air humidity, and O-3. Furthermore, PYR/RCAR proteins seem to function in a dose-dependent manner, and there is a functional diversity among them. Although a rapid stomatal response to elevated CO2 was evident in all but slac1 and ost1 mutants, the bicarbonate-induced activation of S-type anion channels was reduced in the dominant active PP2C mutants abi1-1 and abi2-1. Further experiments with a wider range of CO2 concentrations and analyses of stomatal response kinetics suggested that the ABA signalosome partially affects the CO2-induced stomatal response. Thus, we show that PYR/RCAR receptors play an important role for the whole-plant stomatal adjustments and responses to low humidity, darkness, and O-3 and are involved in responses to elevated CO2.