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Escudero, VAuthorAbreu, IAuthorSopena-Torres, SAuthorMakarovsky-Saavedra, NAuthorGonzalez-Guerrero, MCorresponding AuthorJorda, LCorresponding Author

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February 7, 2022
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Arabidopsis thaliana Zn2+-efflux ATPases HMA2 and HMA4 are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina BMM

Publicated to: Journal Of Experimental Botany. 73 (1): 339-350 - 2022-01-01 73(1), DOI: 10.1093/jxb/erab400

Authors: Escudero, Viviana; Sanchez, Dario Ferreira; Abreu, Isidro; Sopena-Torres, Sara; Makarovsky-Saavedra, Natalia; Bernal, Maria; Kramer, Ute; Grolimund, Daniel; Gonzalez-Guerrero, Manuel; Jorda, Lucia;

Affiliations

Paul Scherrer Inst, Swiss Light Source, MicroXAS Beamline Project, CH-5232 Villigen, Switzerland - Author
Ruhr Univ Bochum, Dept Mol Genet & Physiol Plants, Univ Str, Bochum, Germany - Author
Univ Politecn Madrid, Ctr Biotecnol & Genom Plantes UPM INIA, Inst Nacl Invest & Tecnol Agr & Alimentaria INIA, Pozuelo De Alarcon 28223, Madrid, Spain - Author
Univ Politecn Madrid, Escuela Tecn Super Ingn Agron Alimentaria & Biosi, Dept Biotecnol Biol Vegetal, Madrid 28040, Spain - Author
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Abstract

Zinc is an essential nutrient at low concentrations, but toxic at slightly higher ones. It has been proposed that hyperaccumulator plants may use the excess zinc to fend off pathogens and herbivores. However, there is little evidence of a similar response in other plants. Here we show that Arabidopsis thaliana leaves inoculated with the necrotrophic fungus Plectosphaerella cucumerina BMM (PcBMM) accumulate zinc and manganese at the infection site. Zinc accumulation did not occur in a double mutant in the zinc transporters HEAVY METAL ATPASE2 and HEAVY METAL ATPASE4 (HMA2 and HMA4), which has reduced zinc translocation from roots to shoots. Consistent with a role in plant immunity, expression of HMA2 and HMA4 was up-regulated upon PcBMM inoculation, and hma2hma4 mutants were more susceptible to PcBMM infection. This phenotype was rescued upon zinc supplementation. The increased susceptibility to PcBMM infection was not due to the diminished expression of genes involved in the salicylic acid, ethylene, or jasmonate pathways since they were constitutively up-regulated in hma2hma4 plants. Our data indicate a role of zinc in resistance to PcBMM in plants containing ordinary levels of zinc. This layer of immunity runs in parallel to the already characterized defence pathways, and its removal has a direct effect on resistance to pathogens.

Keywords

Adenosine triphosphatasesArabidopsisArabidopsis proteinsAscomycotaDetoxificationFamilyFull virulenceG-proteinGene expression regulation, plantImmunityInnate immunityIronMembraneMetal transportMicro x-ray fluorescence (mu xrf)Micro x-ray fluorescence (μxrf)PerformanceTransporterZincZinc uptakeZn-atpase

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Journal Of Experimental Botany 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, 2022, it was in position 18/239, 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 from Scopus Elsevier, it yields a value for the Field-Weighted Citation Impact from the Scopus agency: 2.09, which 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)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-12-05, the following number of citations:

  • WoS: 4
  • Scopus: 19

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 2025-12-05:

  • 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: 32.
  • 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: 30 (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: 9.
  • The number of mentions on the social network X (formerly Twitter): 14 (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: https://oa.upm.es/79748/

As a result of the publication of the work in the institutional repository, statistical usage data has been obtained that reflects its impact. In terms of dissemination, we can state that, as of

  • Views: 170
  • Downloads: 102

Leadership analysis of institutional authors

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

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 (ESCUDERO WELSCH, VIVIANA PAMELA) and Last Author (JORDA MIRO, LUCIA).

the authors responsible for correspondence tasks have been GONZALEZ GUERRERO, MANUEL and JORDA MIRO, LUCIA.

Awards linked to the item

This work has been financially supported by the `Severo Ochoa Programme for Centres of Excellence in R&D' from the Agencia Estatal de Investigacion of Spain [grant SEV-2016-0672 (2017-2021) to the CBGP]. In the frame of this program VE was hired with a postdoctoral contract. IA was the recipient of a Juan de la Cierva-Formacion postdoctoral fellowship from Ministerio de Ciencia, Innovacion y Universidades (FJCI-2017-33222).We acknowledge the Paul Scherrer Institut, Villigen, Switzerland for provision of synchrotron radiation beamtime at beamline microXAS, accessed gained through proposals 20190571 and 20180921. The research leading to part of the SXRF data has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement number 730872, project CALIPSOplus.