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Soldek, Joanna NAuthorBallesteros-Gutierrez, MartaAuthorPalacios, Jose ManuelAuthorAlbareda, MartaCorresponding Author

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July 31, 2025
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Two zinc ABC transporters contribute to Rhizobium leguminosarum symbiosis with Pisum sativum and Lens culinaris

Publicated to: Frontiers in Plant Science. 16 1598744- - 2025-06-09 16(), DOI: 10.3389/fpls.2025.1598744

Authors:

Soldek, JN; Ballesteros-Gutiérrez, M; Díaz-Sáez, L; Delgado-Santamaría, I; Palacios, JM; Albareda, M
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Affiliations

CSIC, Inst Quim Fis Blas Cabrera, Madrid, Spain - Author
Univ Politecn Madrid, Ctr Biotecnol & Genomica & Plantas, Inst Nacl Invest & Tecnol Agr & Alimentaria INIA, CSIC, Madrid, Spain - Author
Univ Politecn Madrid, Escuela Tecn Super Ingn Agron Alimentaria & Biosis, Dept Biotecnol Biol Vegetal, Madrid, Spain - Author
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Abstract

The establishment of the rhizobium-legume symbiosis requires adjusting the behavior of both partners to nodule conditions in which transition metals are delivered to the bacteria, as many rhizobial metalloenzymes are essential for bacteroid functions and symbiotic performance. A previous proteomic analysis revealed the existence of a relevant number of proteins differentially expressed in bacteroids induced by Rhizobium leguminosarum bv. viciae (Rlv) UPM791 in pea and lentil nodules. Among these proteins, a metal-binding protein (RLV_3444) component of an ABC-transporter system (RLV_3442-3444) was shown to be overexpressed in pea bacteroids, suggesting that metal provision to the bacteroid is more restrictive in the rhizobium-pea symbiosis. In this work, protein sequence analysis and structural modelling have revealed that RLV_3444 is highly similar to the functionally characterized zinc-binding protein ZniA from Klebsiella pneumoniae, so the host-dependent binding protein was renamed as ZniA and the transporter system as ZniCBA. The genome of Rlv UPM791 also encodes the conserved high-affinity ZnuABC transporter system. We demonstrate that at least one of the two systems must be present for Rlv to grow under zinc-limiting conditions and for optimal symbiotic performance with pea and lentil plants. The three conserved histidine residues present in multiple Zn2+-binding proteins have been shown as essential for the function of Rlv ZniA, and in-silico modelling suggests that they might participate in metal coordination. We also demonstrate that both ZniCBA and ZnuA are regulated by zinc in a Zur-dependent manner, consistent with the presence of a Zur box in their regulatory region. The expression patterns revealed that ZniCBA is expressed at lower levels than ZnuA, and its expression increased in a znuA mutant under both free-living and symbiotic conditions. These results, along with the observed increment in the expression of ZniCBA in pea versus lentil bacteroids, suggest that the host-dependent transporter system might play an auxiliary function for zinc uptake under zinc starvation conditions and might play a relevant role in the adaptation of rhizobia to the legume host.
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Keywords

<italic>rhizobium leguminosarum</italic>Agrobacterium-tumefaciensBv viciaeCrystal-structureEscherichia-coliGene-expressionIn-vitrLegumesLentiLentilMetal-binding propertiesNitrogen fixationNitrogen-fixationPeaRegulator zurRhizobium leguminosarumSymbiosisUptake systemZinc uptake

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Frontiers in Plant Science 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, 2025, it was in position 33/273, thus managing to position itself as a Q1 (Primer Cuartil), in the category Plant Sciences.

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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 2026-04-25:

  • 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: 7.
  • 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: 7 (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: 1.
  • The number of mentions on the social network X (formerly Twitter): 1 (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/92301/

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: 42
  • Downloads: 23
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Leadership analysis of institutional authors

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 (SOLDEK, JOANNA NATALIA) and Last Author (ALBAREDA CONTRERAS, MARTA).

the author responsible for correspondence tasks has been ALBAREDA CONTRERAS, MARTA.

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Awards linked to the item

The author(s) declare that financial support was received for the research and/or publication of this article. This work was supported by a grant from Agencia Estatal de Investigacion, Ministerio de Ciencia e Investigacion (PID2021-124344OB-I100) project to JMP., Spain. JNS was recipient of a Severo Ochoa Program FPI scholarship (PRE2019-090294) from the Ministerio de Ciencia e Investigacion.
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