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Antunez-Lamas, MariaAuthorRodriguez-Palenzuela, PabloAuthorLopez-Solanilla, EmiliaAuthor

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June 9, 2019
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Translocation and Functional Analysis of Pseudomonas savastanoi pv. savastanoi NCPPB 3335 Type III Secretion System Effectors Reveals Two Novel Effector Families of the Pseudomonas syringae Complex

Publicated to: MOLECULAR PLANT-MICROBE INTERACTIONS. 27 (5): 424-436 - 2014-05-01 27(5), DOI: 10.1094/MPMI-07-13-0206-R

Authors:

Matas, IM; Castañeda-Ojeda, MP; Aragón, IM; Antúnez-Lamas, M; Murillo, J; Rodríguez-Palenzuela, P; López-Solanilla, E; Ramos, C
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Affiliations

Interacciones Moleculares Planta-Patógeno. Universidad Politécnica de Madrid - Author
Univ Malaga, Inst Hortofruticultura Subtrop & Mediterranea La, Consejo Super Invest Cient IHSM UMA CSIC, Area Genet,Fac Ciencias - Author
Univ Publ Navarra, Dept Agr Prod, ETS Ingenieros Agronomos - Author
UPM, Dept Biotechnol, Escuela Tecn Super Ingenieros Agronomos - Author
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Abstract

Pseudomonas savastanoi pv. savastanoi NCPPB 3335 causes olive knot disease and is a model pathogen for exploring bacterial infection of woody hosts. The type III secretion system (T3SS) effector repertoire of this strain includes 31 effector candidates plus two novel candidates identified in this study which have not been reported to translocate into plant cells. In this work, we demonstrate the delivery of seven NCPPB 3335 effectors into Nicotiana tabacum leaves, including three proteins from two novel families of the P. syringae complex effector super-repertoire (HopBK and HopBL), one of which comprises two proteins (HopBL1 and HopBL2) that harbor a SUMO protease domain. When delivered by P. fluorescens heterologously expressing a P. syringae T3SS, all seven effectors were found to suppress the production of defense-associated reactive oxygen species. Moreover, six of these effectors, including the truncated versions of HopAA1 and HopAZ1 encoded by NCPPB 3335, suppressed callose deposition. The expression of HopAZ1 and HopBL1 by functionally effectorless P. syringae pv. tomato DC3000D28E inhibited the hypersensitive response in tobacco and, additionally, expression of HopBL2 by this strain significantly increased its competitiveness in N. benthamiana. DNA sequences encoding HopBL1 and HopBL2 were uniquely detected in a collection of 31 P. savastanoi pv. savastanoi strains and other P. syringae strains isolated from woody hosts, suggesting a relevant role of these two effectors in bacterial interactions with olive and other woody plants.
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Keywords

Cysteine protease effectorDisease resistanceHostHypersensitive responseIdentificationLesion formationPathogenProgrammed cell-deathTomato dc3000Virulence determinants

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal MOLECULAR PLANT-MICROBE INTERACTIONS 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, 2014, it was in position 79/290, thus managing to position itself as a Q1 (Primer Cuartil), in the category Biochemistry & Molecular Biology.

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: 1.67, 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 2026-04-28, the following number of citations:

  • WoS: 41
  • Scopus: 40
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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 2026-04-28:

  • 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: 65.
  • 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: 65 (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: 2.
  • The number of mentions on the social network X (formerly Twitter): 2 (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/35893/

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: 342
  • Downloads: 251
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Awards linked to the item

This study was supported by Spanish Plan Nacional I+D+i grants AGL2011-30343-C02-01, AGL2011-30343-C02-02, and AGL2012-32516 from the Ministerio de Economia y Competitividad (MINECO), co-financed by FEDER, and by the grant P08-CVI-03475 from the Junta de Andalucia, Spain. I. M. Matas, I. M. Aragon, and M. P. Castaneda-Ojeda were supported by the Ramon Areces Foundation (Spain) and by FPU and FPI fellowships from the MINECO, respectively. We thank M. Vega Sanchez for excellent assistance with image analysis for quantifying ROS production and callose deposition, L. Santin (University of Malaga, Spain) for statistical analysis of data, and A. Barcelo and I. Imbroda (IFAPA, Churriana, Spain) for micropropagating the olive plants.
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