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This research was supported by the Ministerio de Economia y Competitividad (MINECO) and AEI/FEDER/EU (grants BIO2013-46539-R and BIO2016-80551-R to V.R., and BIO2017-82503-R to P.L.R.); by the Spanish Ministry of Education FPI "Severo Ochoa" fellowships (BES2015071820 to M.G.-L.); by the European Molecular Biology Organization (EMBO) Short-Term programs (ASTF 7678-2016); by the Agence Nationale de Recherche REGLISSE project (ANR-13-ADAP-0008 to L.C.); by an Agencia Espanola de Cooperacion Internacional (AECID) fellowship to D.A.E.-M.; by the Spanish Ministry of Education "Salvador de Madariaga" grant (PRX15/00493 to V.R.); and by Generalitat Valenciana "Programa VALi+d" (APOSTD/2017/039 to B.B.P.). We are thankful to Erika Isono for helpful discussion of the article. We thank Qi Xie for the anti-PYL4 antibody, and Oscar Lorenzo for cra1 seeds. We also thank the confocal microscopy, in vitro plant culture, and greenhouse facilities at the CNB-CSIC for technical support.

Analysis of institutional authors

Rodríguez, LCorresponding Author
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Article

Arabidopsis ALIX Regulates Stomatal Aperture and Turnover of Abscisic Acid Receptors

Publicated to:Plant Cell. 31 (10): 2411-2429 - 2019-10-01 31(10), DOI: 10.1105/tpc.19.00399

Authors: García-León, M; Cuyas, L; Abd El-Moneim, D; Rodriguez, L; Belda-Palazón, B; Sanchez-Quant, E; Fernández, Y; Roux, B; Zamarreño, AM; García-Mina, JM; Nussaume, L; Rodriguez, PL; Paz-Ares, J; Leonhardt, N; Rubio, V

Affiliations

Aix Marseille Univb, Commissariat Energie Atom, CNRS, BIAM,UMR7265,SAVE - Author
Arish Univ, Fac Environm & Agr Sci, Dept Plant Prod, Genet Branch - Author
Ctr Mondial Innovat, Grp Roullier - Author
Ctr Nacl Biotecnol - Author
Helmholtz Zentrum, Helmholtz Pioneer Campus - Author
IST Austria - Author
Univ Navarra, Fac Sci, Dept Environm Biol, Agr Chem & Biol Grp CMI Roullier - Author
Univ Politecn Valencia, Inst Biol Mol & Celular Plantas, CSIC - Author
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Abstract

The plant endosomal trafficking pathway controls the abundance of membrane-associated soluble proteins, as shown for abscisic acid (ABA) receptors of the PYRABACTIN RESISTANCE1/PYR1-LIKE/REGULATORY COMPONENTS OF ABA RECEPTORS (PYR/PYL/RCAR) family. ABA receptor targeting for vacuolar degradation occurs through the late endosome route and depends on FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING1 (FYVE1) and VACUOLAR PROTEIN SORTING23A (VPS23A), components of the ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT-I (ESCRT-I) complexes. FYVE1 and VPS23A interact with ALG-2 INTERACTING PROTEIN-X (ALIX), an ESCRT-III-associated protein, although the functional relevance of such interactions and their consequences in cargo sorting are unknown. In this study we show that Arabidopsis (Arabidopsis thaliana) ALIX directly binds to ABA receptors in late endosomes, promoting their degradation. Impaired ALIX function leads to altered endosomal localization and increased accumulation of ABA receptors. In line with this activity, partial loss-of-function alix-1 mutants display ABA hypersensitivity during growth and stomatal closure, unveiling a role for the ESCRT machinery in the control of water loss through stomata. ABA-hypersensitive responses are suppressed in alix-1 plants impaired in PYR/PYL/RCAR activity, in accordance with ALIX affecting ABA responses primarily by controlling ABA receptor stability. ALIX-1 mutant protein displays reduced interaction with VPS23A and ABA receptors, providing a molecular basis for ABA hypersensitivity in alix-1 mutants. Our findings unveil a negative feedback mechanism triggered by ABA that acts via ALIX to control the accumulation of specific PYR/PYL/RCAR receptors.

Keywords
Aba receptorAbscisic acidAlix protein, arabidopsisArabidopsisArabidopsis proteinArabidopsis proteinsCarrier proteinCarrier proteinsCell surface receptorCell vacuoleChemistryDeubiquitinating enzyme amsh3Drug effectEndosomal sorting complexes required for transportEndosomeEndosomesEscrt proteinEscrt-iiiGeneticsGrowth, development and agingIntracellular signaling peptides and proteinsIntracellular traffickingMembrane transport proteinsMetabolismMultivesicular body pathwayMutationPhytohormonePlant growth regulatorsPlant stomaPlant stomataPlasma-membraneProteinProtein bindingProtein transportReceptors, cell surfaceSignal peptideSignal transductionSorting complexUbiquitinVacuole biogenesisVacuolesWater

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Plant Cell 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, 2019, it was in position 6/234, 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: 1.78. 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 14, 2024)

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: 3.33 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 6.6 (source consulted: Dimensions Apr 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-04-26, the following number of citations:

  • WoS: 41
  • Scopus: 49
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 2025-04-26:

  • 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: 74.
  • 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: 74 (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: 29.68.
  • The number of mentions on the social network Facebook: 4 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 38 (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.
  • Assignment of a Handle/URN as an identifier within the deposit in the Institutional Repository: http://hdl.handle.net/10251/163976
Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Austria; Egypt; France; Germany.

the author responsible for correspondence tasks has been Rodríguez Soriano, Laura.