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Analysis of institutional authors

Fernandez, MaAuthorLozano-Juste, JAuthorRodríguez, LAuthorBueso, EAuthor

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October 30, 2024
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Article

RBR-type E3 ligases and the Ubiquitin-Conjugating Enzyme UBC26 Regulate ABA Receptor Levels and Signaling

Publicated to: PLANT PHYSIOLOGY. 182 (4): 1723-1742 - 2020-01-01 182(4), DOI: 10.1104/pp.19.00898

Authors:

FERNÁNDEZ LÓPEZ, MARIA ANGELES; 0000-0003-4926-1917; Julian J; Coego Gonzalez, Alberto; LOZANO JUSTE, JORGE; Sabrina Iñigo; LESIA RODRIGUEZ; Bueso Rodenas, Eduardo; Alain Goossens; Rodríguez Egea, Pedro Luís; Julian-Valenzuela, Jose
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Affiliations

Uiversidad Politecn Valencia, Inst Biol Mol & Celular Plantas, CSIC - Author
VIB Ctr Plant Syst Biol - Author

Abstract

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. Abscisic acid receptors are targeted for degradation by a family of E3 ubiquitin ligases at different subcellular locations, which modulates hormone signaling in plasma membrane, cytosol, and nucleus
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Keywords

Aba receptorAbscisic acidActivated protein-kinasesArabidopsisArabidopsis proteinArabidopsis proteinsAt1g53025 protein, arabidopsisBiological modelCell fractionationCell nucleusCell surface receptorDegradationGeneticsHhariInsightsMetabolismModels, biologicalMutationPhosphatasesPlant cellPlant cellsPlasma-membranePolyubiquitinationProtein degradationProteolysisPyl4Receptors, cell surfaceRevealsSignal transductionSubcellular fractionsUbiquitin protein ligaseUbiquitin-conjugating enzymesUbiquitin-protein ligasesUbiquitination

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal PLANT PHYSIOLOGY due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2020, it was in position 9/235, thus managing to position itself as a Q1 (Primer Cuartil), in the category Plant Sciences. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 2.3. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 13, 2025)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Weighted Average of Normalized Impact by the Scopus agency: 2.65 (source consulted: FECYT Mar 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2026-04-10, the following number of citations:

  • WoS: 43
  • Scopus: 45
  • Europe PMC: 27
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Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2026-04-10:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 46.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 46 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 14.
  • The number of mentions on the social network Facebook: 3 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 11 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.
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Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Belgium.

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (Fernández Prada, Miguel Ángel) and Last Author (Rodriguez, PL).

the author responsible for correspondence tasks has been Rodriguez, PL.

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Awards linked to the item

This work was supported by the Ministerio de Ciencia, Innovacion y Universidades(MICIU), Fondo Europeo de Desarrollo Regional, and Consejo Superior de Investigaciones Cientificas (grants BIO2014-52537-R and BIO2017-82503-R to P.L.R.), by a Juan de la Cierva contract from MICIU and by the Marie Sklodowska-Curie Action H2020-MSCA-IF-2015-707477 to J.L-J., by Programa VALi1d GVA APOSTD (2017/039 to B.B.-P.), by an FPI contract from MICIU (to J.J.) and by an FPU contract from MECD (to M.A.F.), and by the Belgian Science Policy Organization with postdoctoral fellowships to S.I.
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