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Grant support

We greatly appreciate the donation of some of the lines and constructs used: Dr Heidstra and Dr Scheres (SCZ marker and mutant lines in Col-0 background), Dr Dolf Weiers (ARF5 CDS), Dr Campilho (ahp6-1 and AHP6::GUS) and Dr Ripoll (bdl-2). This study was supported by the Spanish Government (AGL2016-75287-R to CE) and by the Castilla-La Mancha Government (SBPLY/17/180501/000287 to CE). RO was supported by an FPI grant (BES-2014-070108).

Analysis of institutional authors

Del Pozo Benito, Juan CarlosAuthorCabrera, JavierAuthorPernas, MonicaAuthorAngel Moreno-Risueno, MiguelAuthor
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Root-knot nematodes induce gall formation by recruiting developmental pathways of post-embryonic organogenesis and regeneration to promote transient pluripotency

Publicated to:New Phytologist. 227 (1): 200-215 - 2020-07-01 227(1), DOI: 10.1111/nph.16521

Authors: Olmo, Rocio; Cabrera, Javier; Diaz-Manzano, Fernando E.; Ruiz-Ferrer, Virginia; Barcala, Marta; Ishida, Takashi; Garcia, Alejandra; Andres, Maria Fe; Ruiz-Lara, Simon; Verdugo, Isabel; Pernas, Monica; Fukaki, Hidehiro; Carlos del Pozo, Juan; Angel Moreno-Risueno, Miguel; Kyndt, Tina; Gheysen, Godelieve; Fenoll, Carmen; Sawa, Shinichiro; Escobar, Carolina;

Affiliations

CSIC, ICA, Protecc Vegetal, Calle Serrano 115, Madrid 28006, Spain - Author
Inst Nacl Invest & Tecnol Agr & Alimentaria INIA, CBGP, Campus Montegancedo, Madrid 28223, Spain - Author
Kobe Univ, Grad Sch Sci, Dept Biol, 1-1 Rokkodai, Kobe, Hyogo 6578501, Japan - Author
Kumamoto Univ, IROAST, Kumamoto 8608555, Japan - Author
Univ Castilla La Mancha, Area Fisiol Vegetal, Fac Ciencias Ambientales & Bioquim, Avda Carlos III S-N, Toledo 45071, Spain - Author
Univ Ghent, Dept Mol Biotechnol, B-9000 Ghent, Belgium - Author
Univ Talca, Inst Ciencias Biol, Lab Genom Func, Talca 3460000, Chile - Author
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Abstract

Root-knot nematodes (RKNs; Meloidogyne spp.) induce new post-embryogenic organs within the roots (galls) where they stablish and differentiate nematode feeding cells, giant cells (GCs). The developmental programmes and functional genes involved remain poorly defined. Arabidopsis root apical meristem (RAM), lateral root (LR) and callus marker lines, SHORT-ROOT/SHR, SCARECROW/SCR, SCHIZORIZA/SCZ, WUSCHEL-RELATED-HOMEOBOX-5/WOX5, AUXIN-RESPONSIVE-FACTOR-5/ARF5, ARABIDOPSIS-HISTIDINE PHOSPHOTRANSFER-PROTEIN-6/AHP6, GATA-TRANSCRIPTION FACTOR-23/GATA23 and S-PHASE-KINASE-ASSOCIATED-PROTEIN2B/SKP2B, were analysed for nematode-dependent expression. Their corresponding loss-of-function lines, including those for LR upstream regulators, SOLITARY ROOT/SLR/IAA14, BONDELOS/BDL/IAA12 and INDOLE-3-ACETIC-ACID-INDUCIBLE-28/IAA28, were tested for RKN resistance/tolerance. LR genes, for example ARF5 (key factor for root stem-cell niche regeneration), GATA23 (which specifies pluripotent founder cells) and AHP6 (cytokinin-signalling-inhibitor regulating pericycle cell-divisions orientation), show a crucial function during gall formation. RKNs do not compromise the number of founder cells or LR primordia but locally induce gall formation possibly by tuning the auxin/cytokinin balance in which AHP6 might be necessary. Key RAM marker genes were induced and functional in galls. Therefore, the activation of plant developmental programmes promoting transient-pluripotency/stemness leads to the generation of quiescent-centre and meristematic-like cell identities within the vascular cylinder of galls. Nematodes enlist developmental pathways of new organogenesis and/or root regeneration in the vascular cells of galls. This should determine meristematic cell identities with sufficient transient pluripotency for gall organogenesis.

Keywords
auxinscallicytokininsgall developmentlateral rootmeloidogyne spp.pluripotencyActivationArabidopsisAuxinAuxinsCalliCallus formationCytokininsF-boxGall developmentGene-expressionHeat-shockLateral rootMeloidogyne sppMeloidogyne spp.Meloidogyne-javanicaPlantPluripotencyRegenerationRoot meristemRoot meristem/regeneration

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal New Phytologist 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 7/235, 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: 1.42. 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: 3.44 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 7.43 (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: 18
  • Scopus: 42
  • OpenCitations: 43
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: 79.
  • 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: 79 (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: 13.7.
  • The number of mentions on the social network X (formerly Twitter): 25 (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.
Leadership analysis of institutional authors

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