Publications by authors named "Jesús Mercado-Blanco"

39 Publications

Coupling the endophytic microbiome with the host transcriptome in olive roots.

Comput Struct Biotechnol J 2021 21;19:4777-4789. Epub 2021 Aug 21.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, CSIC, Campus 'Alameda del Obispo' s/n, Avd. Menéndez Pidal s/n, 14004 Córdoba, Spain.

The connection between olive genetic responses to environmental and agro-climatic conditions and the composition, structure and functioning of host-associated, belowground microbiota has never been studied under the holobiont conceptual framework. Two groups of cultivars growing under the same environmental, pedological and agronomic conditions, and showing highest (AH) and lowest (AL) relative abundances, were earlier identified. We aimed now to: i) compare the root transcriptome profiles of these two groups harboring significantly different relative abundances in the above-mentioned bacterial genus; ii) examine their rhizosphere and root-endosphere microbiota co-occurrence networks; and iii) connect the root host transcriptome pattern to the composition of the root microbial communities by correlation and co-occurrence network analyses. Significant differences in olive gene expression were found between the two groups. Co-occurrence networks of the root endosphere microbiota were clearly different as well. Pearson's correlation analysis enabled a first portray of the interaction occurring between the root host transcriptome and the endophytic community. To further identify keystone operational taxonomic units (OTUs) and genes, subsequent co-occurrence network analysis showed significant interactions between 32 differentially expressed genes (DEGs) and 19 OTUs. Overall, negative correlation was detected between all upregulated genes in the AH group and all OTUs except of . While two groups of olive cultivars grown under the same conditions showed significantly different microbial profiles, the most remarkable finding was to unveil a strong correlation between these profiles and the differential gene expression pattern of each group. In conclusion, this study shows a holistic view of the plant-microbiome communication.
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http://dx.doi.org/10.1016/j.csbj.2021.08.035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8411203PMC
August 2021

Evaluation of Indigenous Olive Biocontrol Rhizobacteria as Protectants against Drought and Salt Stress.

Microorganisms 2021 Jun 3;9(6). Epub 2021 Jun 3.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Avenida Menéndez Pidal s/n, Campus "Alameda del Obispo", 14004 Córdoba, Spain.

Stress caused by drought and salinity may compromise growth and productivity of olive ( L.) tree crops. Several studies have reported the use of beneficial rhizobacteria to alleviate symptoms produced by these stresses, which is attributed in some cases to the activity of 1-aminocyclopropane-1-carboxylic acid deaminase (ACD). A collection of beneficial olive rhizobacteria was in vitro screened for ACD activity. sp. PICF6 displayed this phenotype and sequencing of its genome confirmed the presence of an gene. In contrast, the well-known root endophyte and biocontrol agent PICF7 was defective in ACD activity, even though the presence of an ACD-coding gene was earlier predicted in its genome. In this study, an unidentified deaminase was confirmed instead. Greenhouse experiments with olive 'Picual' plants inoculated either with PICF6 or PICF7, or co-inoculated with both strains, and subjected to drought or salt stress were carried out. Several physiological and biochemical parameters increased in stressed plants (i.e., stomatal conductance and flavonoids content), regardless of whether or not they were previously bacterized. Results showed that neither PICF6 (ACD positive) nor PICF7 (ACD negative) lessened the negative effects caused by the abiotic stresses tested, at least under our experimental conditions.
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http://dx.doi.org/10.3390/microorganisms9061209DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8230297PMC
June 2021

Functional Traits of Olive Varieties and Their Relationship with the Tolerance Level towards Verticillium Wilt.

Plants (Basel) 2021 May 27;10(6). Epub 2021 May 27.

Departamento de Botánica, Ecología y Fisiología Vegetal, Universidad de Córdoba, Campus Universitario de Rabanales, 14014 Córdoba, Spain.

Verticillium wilt of olive (VWO), caused by the soil-borne pathogen is considered one of the most important diseases affecting this tree crop. One of the best VWO management measures is the use of tolerant cultivars. Remarkably, no information is available about olive functional traits and their potential relationship with tolerance to . Twenty-five selected functional traits (for leaf, stem, root and whole plant) were evaluated in six olive varieties differing in their VWO tolerance level to identify possible links between this phenotype and functional traits' variation. High intervarietal diversity was found among cultivars and several functional traits were related with VWO tolerance. Tolerant varieties showed higher leaf area, dry matter content (leaf, stem and plant) and mass fraction for stems, but lower for leaves. Significant differences were also detected for root functional traits, tolerant cultivars displaying larger fine root diameter and lignin content but smaller specific length and area of thick and fine roots. Correlations were found among functional traits both within varieties and between levels of tolerance/susceptibility to VWO. Associations were observed between biomass allocation, dry matter content and VWO tolerance. The most relevant difference between tolerant and susceptible cultivars was related to root system architecture.
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http://dx.doi.org/10.3390/plants10061079DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8230176PMC
May 2021

The Banana Root Endophytome: Differences between Mother Plants and Suckers and Evaluation of Selected Bacteria to Control f.sp. .

J Fungi (Basel) 2021 Mar 9;7(3). Epub 2021 Mar 9.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, Consejo Superior de Investigaciones Científicas (CSIC), Campus 'Alameda del Obispo' s/n, Avd. Menéndez Pidal s/n, 14004 Córdoba, Spain.

This study aimed to disentangle the structure, composition, and co-occurrence relationships of the banana (cv. Dwarf Cavendish) root endophytome comparing two phenological plant stages: mother plants and suckers. Moreover, a collection of culturable root endophytes (>1000) was also generated from Canary Islands. In vitro antagonism assays against f.sp. () races STR4 and TR4 enabled the identification and characterization of potential biocontrol agents (BCA). Eventually, three of them were selected and evaluated against Fusarium wilt of banana (FWB) together with the well-known BCA PICF7 under controlled conditions. Culturable and non-culturable (high-throughput sequencing) approaches provided concordant information and showed low microbial diversity within the banana root endosphere. appeared as the dominant genus and seemed to play an important role in the banana root endophytic microbiome according to co-occurrence networks. Fungal communities were dominated by the genera and . Overall, significant differences were found between mother plants and suckers, suggesting that the phenological stage determines the recruitment and organization of the endophytic microbiome. While selected native banana endophytes showed clear antagonism against strains, their biocontrol performance against FWB did not improve the outcome observed for a non-indigenous reference BCA (strain PICF7).
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http://dx.doi.org/10.3390/jof7030194DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8002102PMC
March 2021

Verticillium wilt resistant and susceptible olive cultivars express a very different basal set of genes in roots.

BMC Genomics 2021 Apr 1;22(1):229. Epub 2021 Apr 1.

Department of Experimental Biology, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jaén, 23071, Jaén, Spain.

Background: Olive orchards are threatened by a wide range of pathogens. Of these, Verticillium dahliae has been in the spotlight for its high incidence, the difficulty to control it and the few cultivars that has increased tolerance to the pathogen. Disease resistance not only depends on detection of pathogen invasion and induction of responses by the plant, but also on barriers to avoid the invasion and active resistance mechanisms constitutively expressed in the absence of the pathogen. In a previous work we found that two healthy non-infected plants from cultivars that differ in V. dahliae resistance such as 'Frantoio' (resistant) and 'Picual' (susceptible) had a different root morphology and gene expression pattern. In this work, we have addressed the issue of basal differences in the roots between Resistant and Susceptible cultivars.

Results: The gene expression pattern of roots from 29 olive cultivars with different degree of resistance/susceptibility to V. dahliae was analyzed by RNA-Seq. However, only the Highly Resistant and Extremely Susceptible cultivars showed significant differences in gene expression among various groups of cultivars. A set of 421 genes showing an inverse differential expression level between the Highly Resistant to Extremely Susceptible cultivars was found and analyzed. The main differences involved higher expression of a series of transcription factors and genes involved in processes of molecules importation to nucleus, plant defense genes and lower expression of root growth and development genes in Highly Resistant cultivars, while a reverse pattern in Moderately Susceptible and more pronounced in Extremely Susceptible cultivars were observed.

Conclusion: According to the different gene expression patterns, it seems that the roots of the Extremely Susceptible cultivars focus more on growth and development, while some other functions, such as defense against pathogens, have a higher expression level in roots of Highly Resistant cultivars. Therefore, it seems that there are constitutive differences in the roots between Resistant and Susceptible cultivars, and that susceptible roots seem to provide a more suitable environment for the pathogen than the resistant ones.
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http://dx.doi.org/10.1186/s12864-021-07545-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8017696PMC
April 2021

Assessing the Involvement of Selected Phenotypes of PICF7 in Olive Root Colonization and Biological Control of .

Plants (Basel) 2021 Feb 23;10(2). Epub 2021 Feb 23.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Avenida Menéndez Pidal s/n, Campus "Alameda del Obispo", 14004 Córdoba, Spain.

PICF7 is an indigenous inhabitant of the olive ( L.) rhizosphere/root endosphere and an effective biocontrol agent against Verticillium wilt of olive (VWO), caused by the soil-borne fungus . This study aimed to evaluate the potential involvement of selected phenotypes of strain PICF7 in root colonization ability and VWO biocontrol. Therefore, a random transposon-insertion mutant bank of PICF7 was screened for the loss of phenotypes likely involved in rhizosphere/soil persistence (copper resistance), root colonization (biofilm formation) and plant growth promotion (phytase activity). Transposon insertions in genes putatively coding for the transcriptional regulator CusR or the chemotaxis protein CheV were found to affect copper resistance, whereas an insertion in gene putatively encoding a flagellar regulatory protein hampered the ability to form a biofilm. However, these mutants displayed the same antagonistic effect against as the parental strain. Remarkably, two mutants impaired in biofilm formation were never found inside olive roots, whereas their ability to colonize the root exterior and to control VWO remained unaffected. Endophytic colonization of olive roots was unaltered in mutants impaired in copper resistance and phytase production. Results demonstrated that the phenotypes studied were irrelevant for VWO biocontrol.
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http://dx.doi.org/10.3390/plants10020412DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7926765PMC
February 2021

Comparative study of neighboring Holm oak and olive trees-belowground microbial communities subjected to different soil management.

PLoS One 2020 11;15(8):e0236796. Epub 2020 Aug 11.

Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Granada, Spain.

It is well-known that different plant species, and even plant varieties, promote different assemblages of the microbial communities associated with them. Here, we investigate how microbial communities (bacteria and fungi) undergo changes within the influence of woody plants (two olive cultivars, one tolerant and another susceptible to the soilborne fungal pathogen Verticillium dahliae, plus wild Holm oak) grown in the same soil but with different management (agricultural versus native). By the use of metabarcoding sequencing we determined that the native Holm oak trees rhizosphere bacterial communities were different from its bulk soil, with differences in some genera like Gp4, Gp6 and Solirubrobacter. Moreover, the agricultural management used in the olive orchard led to belowground microbiota differences with respect to the natural conditions both in bulk soils and rhizospheres. Indeed, Gemmatimonas and Fusarium were more abundant in olive orchard soils. However, agricultural management removed the differences in the microbial communities between the two olive cultivars, and these differences were minor respect to the olive bulk soil. According to our results, and at least under the agronomical conditions here examined, the composition and structure of the rhizospheric microbial communities do not seem to play a major role in olive tolerance to V. dahliae.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0236796PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7418964PMC
October 2020

Epigenetic Regulation of Virulence: Does DNA Methylation Level Play A Role?

Int J Mol Sci 2020 Jul 22;21(15). Epub 2020 Jul 22.

Center for Advanced Studies in Olive Grove and Olive Oils, Department of Experimental Biology, Univ. Jaén, 23071 Jaén, Spain.

is the etiological agent of Verticillium wilt of olive. The virulence of Defoliating isolates usually displays differences and high plasticity. This work studied whether an epigenetic mechanism was involved in this plasticity. An inverse correlation between virulence and DNA methylation of protein-coding genes was found. A set of 831 genes was selected for their highly consistent inverse methylation profile and virulence in the five studied isolates. Of these genes, ATP-synthesis was highly represented, which indicates that the more virulent D isolates are, the more energy requirements they may have. Furthermore, there were numerous genes in the protein biosynthesis process: genes coding for the chromatin structure, which suggests that epigenetic changes may also affect chromatin condensation; many transmembrane transporter genes, which is consistent with denser compounds, traffic through membranes in more virulent isolates; a fucose-specific lectin that may play a role in the attachment to plant cell walls during the host infection process; and pathogenic cutinases that facilitate plant invasion and sporulation genes for rapid spreading alongside plants. Our findings support the notion that differences in the virulence of the Defoliating isolates may be controlled, at least to some extent, by an epigenetic mechanism.
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http://dx.doi.org/10.3390/ijms21155197DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7432615PMC
July 2020

Verticillium Wilt of Olive and its Control: What Did We Learn during the Last Decade?

Plants (Basel) 2020 Jun 11;9(6). Epub 2020 Jun 11.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible (IAS), Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Avenida Menéndez Pidal s/n, Campus "Alameda del Obispo", 14004 Córdoba, Spain.

Verticillium ( Kleb.) wilt is one of the most devastating diseases affecting olive ( L. subsp. var. a) cultivation. Its effective control strongly relies on integrated management strategies. Olive cultivation systems are experiencing important changes (e.g., high-density orchards, etc.) aiming at improving productivity. The impact of these changes on soil biology and the incidence/severity of olive pests and diseases has not yet been sufficiently evaluated. A comprehensive understanding of the biology of the pathogen and its populations, the epidemiological factors contributing to exacerbating the disease, the underlying mechanisms of tolerance/resistance, and the involvement of the olive-associated microbiota in the tree's health is needed. This knowledge will be instrumental to developing more effective control measures to confront the disease in regions where the pathogen is present, or to exclude it from -free areas. This review compiles the most recent advances achieved to understand the olive- interaction as well as measures to control the disease. Aspects such as the molecular basis of the host-pathogen interaction, the identification of new biocontrol agents, the implementation of "-omics" approaches to unravel the basis of disease tolerance, and the utilization of remote sensing technology for the early detection of pathogen attacks are highlighted.
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http://dx.doi.org/10.3390/plants9060735DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7356185PMC
June 2020

Linking belowground microbial network changes to different tolerance level towards Verticillium wilt of olive.

Microbiome 2020 02 1;8(1):11. Epub 2020 Feb 1.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, CSIC, Campus 'Alameda del Obispo' s/n, Avd. Menéndez Pidal s/n, 14004, Córdoba, Spain.

Background: Verticillium wilt of olive (VWO) is caused by the soilborne fungal pathogen Verticillium dahliae. One of the best VWO management measures is the use of tolerant/resistant olive cultivars. Knowledge on the olive-associated microbiome and its potential relationship with tolerance to biotic constraints is almost null. The aims of this work are (1) to describe the structure, functionality, and co-occurrence interactions of the belowground (root endosphere and rhizosphere) microbial communities of two olive cultivars qualified as tolerant (Frantoio) and susceptible (Picual) to VWO, and (2) to assess whether these communities contribute to their differential disease susceptibility level.

Results: Minor differences in alpha and beta diversities of root-associated microbiota were detected between olive cultivars regardless of whether they were inoculated or not with the defoliating pathotype of V. dahliae. Nevertheless, significant differences were found in taxonomic composition of non-inoculated plants' communities, "Frantoio" showing a higher abundance of beneficial genera in contrast to "Picual" that exhibited major abundance of potential deleterious genera. Upon inoculation with V. dahliae, significant changes at taxonomic level were found mostly in Picual plants. Relevant topological alterations were observed in microbial communities' co-occurrence interactions after inoculation, both at structural and functional level, and in the positive/negative edges ratio. In the root endosphere, Frantoio communities switched to highly connected and low modularized networks, while Picual communities showed a sharply different behavior. In the rhizosphere, V. dahliae only irrupted in the microbial networks of Picual plants.

Conclusions: The belowground microbial communities of the two olive cultivars are very similar and pathogen introduction did not provoke significant alterations in their structure and functionality. However, notable differences were found in their networks in response to the inoculation. This phenomenon was more evident in the root endosphere communities. Thus, a correlation between modifications in the microbial networks of this microhabitat and susceptibility/tolerance to a soilborne pathogen was found. Moreover, V. dahliae irruption in the Picual microbial networks suggests a stronger impact on the belowground microbial communities of this cultivar upon inoculation. Our results suggest that changes in the co-occurrence interactions may explain, at least partially, the differential VWO susceptibility of the tested olive cultivars. Video abstract.
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http://dx.doi.org/10.1186/s40168-020-0787-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6995654PMC
February 2020

Defining the root endosphere and rhizosphere microbiomes from the World Olive Germplasm Collection.

Sci Rep 2019 12 31;9(1):20423. Epub 2019 Dec 31.

Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Calle Profesor Albareda 1, 18008, Granada, Spain.

The bacterial and fungal communities from the olive (Olea europaea L.) root systems have not yet been simultaneously studied. We show in this work that microbial communities from the olive root endosphere are less diverse than those from the rhizosphere. But more relevant was to unveil that olive belowground communities are mainly shaped by the genotype of the cultivar when growing under the same environmental, pedological and agronomic conditions. Furthermore, Actinophytocola, Streptomyces and Pseudonocardia are the most abundant bacterial genera in the olive root endosphere, Actinophytocola being the most prevalent genus by far. In contrast, Gp6, Gp4, Rhizobium and Sphingomonas are the main genera in the olive rhizosphere. Canalisporium, Aspergillus, Minimelanolocus and Macrophomina are the main fungal genera present in the olive root system. Interestingly enough, a large number of as yet unclassified fungal sequences (class level) were detected in the rhizosphere. From the belowground microbial profiles here reported, it can be concluded that the genus Actinophytocola may play an important role in olive adaptation to environmental stresses. Moreover, the huge unknown fungal diversity here uncovered suggests that fungi with important ecological function and biotechnological potential are yet to be identified.
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http://dx.doi.org/10.1038/s41598-019-56977-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6938483PMC
December 2019

Editorial: Harnessing Useful Rhizosphere Microorganisms for Pathogen and Pest Biocontrol - Second Edition.

Front Microbiol 2019 28;10:1935. Epub 2019 Aug 28.

Instituto de Agricultura Sostenible, Agencia Estatal Consejo Superior de Investigaciones Científicas, Córdoba, Spain.

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http://dx.doi.org/10.3389/fmicb.2019.01935DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6724568PMC
August 2019

Corrigendum: Biological Control Agents Against Fusarium Wilt of Banana.

Front Microbiol 2019 11;10:1290. Epub 2019 Jun 11.

Department of Crop Protection, Institute for Sustainable Agriculture (CSIC), Córdoba, Spain.

[This corrects the article DOI: 10.3389/fmicb.2019.00616.].
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http://dx.doi.org/10.3389/fmicb.2019.01290DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580181PMC
June 2019

Efficient colonization of the endophytes Herbaspirillum huttiense RCA24 and Enterobacter cloacae RCA25 influences the physiological parameters of Oryza sativa L. cv. Baldo rice.

Environ Microbiol 2019 May 20. Epub 2019 May 20.

Institute of Biosciences and BioResources, via P. Castellino 111, 80131 Naples, Italy.

Several important bacterial characteristics, such as biological nitrogen fixation, phosphate solubilisation, 1-aminocyclopropane-1-carboxylate deaminase activity, and production of siderophores and phytohormones, can be assessed as plant growth promotion traits. Our aim was to evaluate the effects of nitrogen-fixing and indole-3-acetic acid (IAA) producing endophytes in two Oryza sativa cultivars (Baldo and Vialone Nano). Three bacteria, Herbaspirillum huttiense RCA24, Enterobacter asburiae RCA23 and Staphylococcus sp. 377, producing different IAA levels, were tested for their ability to enhance nifH gene expression and nitrogenase activity in Enterobacter cloacae RCA25. Results showed that H. huttiense RCA24 performed best. Improvement in nitrogen-fixation and changes in physiological parameters such as chlorophyll, nitrogen content and shoot dry weight were observed for plants co-inoculated with strains RCA25 and RCA24 in a 10:1 ratio. Based on confocal laser scanning microscopy analysis, strain RCA24 was the best colonizer of the root interior and the only IAA producer located in the same root niche occupied by RCA25 cells. This work shows that the choice of a bio-inoculum having the right composition is one of the key aspects to be considered for the inoculation of a specific host plant cultivar with microbial consortia. This article is protected by copyright. All rights reserved.
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http://dx.doi.org/10.1111/1462-2920.14688DOI Listing
May 2019

Biological Control Agents Against Fusarium Wilt of Banana.

Front Microbiol 2019 5;10:616. Epub 2019 Apr 5.

Department of Crop Protection, Institute for Sustainable Agriculture (CSIC), Córdoba, Spain.

In the last century, the banana crop and industry experienced dramatic losses due to an epidemic of Fusarium wilt of banana (FWB), caused by f.sp. () race 1. An even more dramatic menace is now feared due to the spread of tropical race 4. Plant genetic resistance is generally considered as the most plausible strategy for controlling effectively such a devastating disease, as occurred for the first round of FWB epidemic. Nevertheless, with at least 182 articles published since 1970, biological control represents a large body of knowledge on FWB. Remarkably, many studies deal with biological control agents (BCAs) that reached the field-testing stage and even refer to high effectiveness. Some selected BCAs have been repeatedly assayed in independent trials, suggesting their promising value. Overall under field conditions, FWB has been controlled up to 79% by using spp. strains, and up to 70% by several endophytes and spp. strains. Lower biocontrol efficacy (42-55%) has been obtained with arbuscular mycorrhizal fungi, spp., and non-pathogenic strains. Studies on spp. have been mostly limited to conditions so far, with very few pot-experiments, and none conducted in the field. The BCAs have been applied with diverse procedures (e.g., spore suspension, organic amendments, bioformulations, etc.) and at different stages of plant development (i.e., , nursery, at transplanting, post-transplanting), but there has been no evidence for a protocol better than another. Nonetheless, new bioformulation technologies (e.g., nanotechnology, formulation of microbial consortia and/or their metabolites, etc.) and tailor-made consortia of microbial strains should be encouraged. In conclusion, the literature offers many examples of promising BCAs, suggesting that biocontrol can greatly contribute to limit the damage caused by FWB. More efforts should be done to further validate the currently available outcomes, to deepen the knowledge on the most valuable BCAs, and to improve their efficacy by setting up effective formulations, application protocols, and integrated strategies.
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http://dx.doi.org/10.3389/fmicb.2019.00616DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6459961PMC
April 2019

The Transcriptome of Responds Differentially Depending on the Disease Susceptibility Level of the Olive ( L.) Cultivar.

Genes (Basel) 2019 03 27;10(4). Epub 2019 Mar 27.

Department of Crop Protection, Institute for Sustainable Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Campus 'Alameda del Obispo', Avenida Menéndez Pidal s/n, 14004 Córdoba, Spain.

Among biotic constraints affecting olive trees cultivation worldwide, the soil-borne fungus is considered one of the most serious threats. Olive cultivars display differential susceptibility to the disease, but our knowledge on the pathogen's responses when infecting varieties differing in susceptibility is scarce. A comparative transcriptomic analysis (RNA-seq) was conducted in olive cultivars Picual (susceptible) and Frantoio (tolerant). RNA samples originated from roots during the first two weeks after inoculation with defoliating (D) pathotype. mRNA amount was overwhelmingly higher in roots of the susceptible cultivar, indicating that proliferation of pathogen biomass is favored in 'Picual'. A significant larger number of unigenes (11 fold) were only induced in this cultivar. Seven clusters of differentially expressed genes (DEG) were identified according to time-course expression patterns. Unigenes potentially coding for niche-adaptation, pathogenicity, virulence and microsclerotia development were induced in 'Picual', while in 'Frantoio' expression remained negligible or null. D pathotype transcriptome responses are qualitatively and quantitatively different, and depend on cultivar susceptibility level. The much larger biomass found in 'Picual' roots is a consequence of both host and pathogen DEG explaining, to a large extent, the higher aggressiveness exerted over this cultivar.
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http://dx.doi.org/10.3390/genes10040251DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6523120PMC
March 2019

Belowground Microbiota and the Health of Tree Crops.

Front Microbiol 2018 5;9:1006. Epub 2018 Jun 5.

Centre for Mechanical Engineering, Materials and Processes (CEMMPRE) and Department of Life Sciences, University of Coimbra, Coimbra, Portugal.

Trees are crucial for sustaining life on our planet. Forests and land devoted to tree crops do not only supply essential edible products to humans and animals, but also additional goods such as paper or wood. They also prevent soil erosion, support microbial, animal, and plant biodiversity, play key roles in nutrient and water cycling processes, and mitigate the effects of climate change acting as carbon dioxide sinks. Hence, the health of forests and tree cropping systems is of particular significance. In particular, soil/rhizosphere/root-associated microbial communities (known as microbiota) are decisive to sustain the fitness, development, and productivity of trees. These benefits rely on processes aiming to enhance nutrient assimilation efficiency (plant growth promotion) and/or to protect against a number of (a)biotic constraints. Moreover, specific members of the microbial communities associated with perennial tree crops interact with soil invertebrate food webs, underpinning many density regulation mechanisms. This review discusses belowground microbiota interactions influencing the growth of tree crops. The study of tree-(micro)organism interactions taking place at the belowground level is crucial to understand how they contribute to processes like carbon sequestration, regulation of ecosystem functioning, and nutrient cycling. A comprehensive understanding of the relationship between roots and their associate microbiota can also facilitate the design of novel sustainable approaches for the benefit of these relevant agro-ecosystems. Here, we summarize the methodological approaches to unravel the composition and function of belowground microbiota, the factors influencing their interaction with tree crops, their benefits and harms, with a focus on representative examples of Biological Control Agents (BCA) used against relevant biotic constraints of tree crops. Finally, we add some concluding remarks and suggest future perspectives concerning the microbiota-assisted management strategies to sustain tree crops.
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http://dx.doi.org/10.3389/fmicb.2018.01006DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5996133PMC
June 2018

Indigenous spp. Strains from the Olive ( L.) Rhizosphere as Effective Biocontrol Agents against : From the Host Roots to the Bacterial Genomes.

Front Microbiol 2018 23;9:277. Epub 2018 Feb 23.

Department of Crop Protection, Institute for Sustainable Agriculture (CSIC), Córdoba, Spain.

The use of biological control agents (BCA), alone or in combination with other management measures, has gained attention over the past decades, driven by the need to seek for sustainable and eco-friendly alternatives to confront plant pathogens. The rhizosphere of olive ( L.) plants is a source of bacteria with potential as biocontrol tools against Verticillium wilt of olive (VWO) caused by Kleb. A collection of bacterial isolates from healthy nursery-produced olive (cultivar Picual, susceptible to VWO) plants was generated based on morphological, biochemical and metabolic characteristics, chemical sensitivities, and on their antagonistic activity against several olive pathogens. Three strains (PIC25, PIC105, and PICF141) showing high inhibition ability of pathogens' growth, particularly against , were eventually selected. Their effectiveness against VWO caused by the defoliating pathotype of was also demonstrated, strain PICF141 being the rhizobacteria showing the best performance as BCA. Genotypic and phenotypic traits traditionally associated with plant growth promotion and/or biocontrol abilities were evaluated as well (e.g., phytase, xylanase, catalase, cellulase, chitinase, glucanase activities, and siderophore and HCN production). Multi-locus sequence analyses of conserved genes enabled the identification of these strains as spp. Strain PICF141 was affiliated to the " subgroup," within the " group," being the closest species. Strains PIC25 and PIC105 were affiliated to the " group," being the closest relative. Moreover, we identified (PIC105) for the first time as a BCA. Genome sequencing and analyses allowed the identification of traits commonly associated with plant-bacteria interactions. Finally, the root colonization ability of these olive rhizobacteria was assessed, providing valuable information for the future development of formulations based on these strains. A set of actions, from rhizosphere isolation to genome analysis, is proposed and discussed for selecting indigenous rhizobacteria as effective BCAs.
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http://dx.doi.org/10.3389/fmicb.2018.00277DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5829093PMC
February 2018

Tolerance of olive (Olea europaea) cv Frantoio to Verticillium dahliae relies on both basal and pathogen-induced differential transcriptomic responses.

New Phytol 2018 01 12;217(2):671-686. Epub 2017 Oct 12.

Department of Crop Protection, Institute for Sustainable Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Campus 'Alameda del Obispo', Avenida Menéndez Pidal s/n, Apartado, Córdoba, 14004, Spain.

Verticillium wilt of olive (VWO) is one of the most serious biotic constraints for this tree crop. Our knowledge of the genetics of the tolerance/resistance to this disease is very limited. Here we show that tolerance of the cv Frantoio relies on both basal and early pathogen-induced differential transcriptomic responses. A comparative transcriptomic analysis (RNA-seq) was conducted in root tissues of cvs Frantoio (VWO-tolerant) and Picual (VWO-susceptible). RNA samples originated from roots of inoculated olive plants during the early infection stages by Verticillium dahliae (highly virulent, defoliating pathotype). A huge number of differentially expressed genes (DEGs) were found between 'Frantoio' and 'Picual' (27 312 unigenes) in the absence of the pathogen. Upon infection with V. dahliae, 'Picual' and 'Frantoio' plants responded differently too. In the early infection stages, four clusters of DEGs could be identified according to their time-course expression patterns. Among others, a pathogenesis-related protein of the Bet v I family and a dirigent-like protein involved in lignification, and several BAK1, NHL1, reactive oxygen species stress response and BAM unigenes showed noticeable differences between cultivars. Tolerance of 'Frantoio' plants to VWO is a consequence of a complex and multifaceted process which involves many plant traits.
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http://dx.doi.org/10.1111/nph.14833DOI Listing
January 2018

Transcriptomic Analysis of L. Roots during the Early Infection Process.

Plant Genome 2017 03;10(1)

Olive cultivation is affected by a wide range of biotic constraints. Verticillium wilt of olive is one of the most devastating diseases affecting this woody crop, inflicting major economic losses in many areas, particularly within the Mediterranean Basin. Little is known about gene-expression changes during plant infection by of woody plants such as olive. A complete RNA-seq transcriptomic analysis of olive tree roots was made. Trinity assembler proved to be the best option to assemble the olive and transcriptomes. The olive transcriptome (Oleup) consisted of 68,259 unigenes (254,252 isoforms/transcripts), and the transcriptome (Vedah) consisted of 37,425 unigenes (52,119 isoforms/transcripts). Most unigenes of the Oleup transcriptome corresponded to cellular processes (12,339), metabolic processes (10,974), single-organism processes (7263), and responses to stimuli (5114). As for the Vedah transcriptome, most unigenes correspond to metabolic processes (25,372), cellular processes (23,718), localization (6385), and biological regulation (4801). Differential gene-expression analysis of both transcriptomes was made at 2 and 7 d post-infection. The induced genes of both organisms during the plant-pathogen interaction were clustered in six subclusters, depending on the expression patterns during the infection. Subclusters A to C correspond to plant genes, and subcluster D to F correspond to genes. A relevant finding was that the differentially expressed gene (DEGs) included in subclusters B and C were highly enriched in proteolysis as well as protein-folding and biosynthesis genes. In addition, a reactive oxygen species (ROS) defense was induced first in the pathogen and later in the plant roots.
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http://dx.doi.org/10.3835/plantgenome2016.07.0060DOI Listing
March 2017

Editorial: Harnessing Useful Rhizosphere Microorganisms for Pathogen and Pest Biocontrol.

Front Microbiol 2016 19;7:1620. Epub 2016 Oct 19.

Instituto Agricultura Sostenible, Agencia Estatal Consejo Superior de Investigaciones Científicas Córdoba, Spain.

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http://dx.doi.org/10.3389/fmicb.2016.01620DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5069421PMC
October 2016

Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X940.

Environ Microbiol 2016 10 27;18(10):3522-3534. Epub 2016 Jun 27.

Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Cuidad Autónoma de Buenos Aires, Buenos Aires, Argentina.

A main goal of biological nitrogen fixation research has been to expand the nitrogen-fixing ability to major cereal crops. In this work, we demonstrate the use of the efficient nitrogen-fixing rhizobacterium Pseudomonas protegens Pf-5 X940 as a chassis to engineer the transfer of nitrogen fixed by BNF to maize and wheat under non-gnotobiotic conditions. Inoculation of maize and wheat with Pf-5 X940 largely improved nitrogen content and biomass accumulation in both vegetative and reproductive tissues, and this beneficial effect was positively associated with high nitrogen fixation rates in roots. N isotope dilution analysis showed that maize and wheat plants obtained substantial amounts of fixed nitrogen from the atmosphere. Pf-5 X940-GFP-tagged cells were always reisolated from the maize and wheat root surface but never from the inner root tissues. Confocal laser scanning microscopy confirmed root surface colonization of Pf-5 X940-GFP in wheat plants, and microcolonies were mostly visualized at the junctions between epidermal root cells. Genetic analysis using biofilm formation-related Pseudomonas mutants confirmed the relevance of bacterial root adhesion in the increase in nitrogen content, biomass accumulation and nitrogen fixation rates in wheat roots. To our knowledge, this is the first report of robust BNF in major cereal crops.
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http://dx.doi.org/10.1111/1462-2920.13376DOI Listing
October 2016

Pseudomonas fluorescens PICF7 displays an endophytic lifestyle in cultivated cereals and enhances yield in barley.

FEMS Microbiol Ecol 2016 08 28;92(8). Epub 2016 Apr 28.

Plant Breeding, Institute for Sustainable Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Avda Menéndez Pidal s/n, Campus Alameda del Obispo s/n, E-14004 Córdoba, Spain

Pseudomonas fluorescens PICF7, an indigenous inhabitant of olive roots, displays an endophytic lifestyle in this woody crop and exerts biocontrol against the fungal phytopathogen Verticillium dahliae Here we report microscopy evidence that the strain PICF7 is also able to colonize and persist on or in wheat and barley root tissues. Root colonization of both cereal species followed a similar pattern to that previously reported in olive, including inner colonization of the root hairs. This demonstrates that strain PICF7 can colonize root systems of distant botanical species. Barley plants germinated from PICF7-treated seeds showed enhanced vegetative growth. Moreover, significant increases in the number of grains (up to 19.5%) and grain weight (up to 20.5%) per plant were scored in this species. In contrast, growth and yield were not significantly affected in wheat plants by the presence of PICF7. Proteomics analysis of the root systems revealed that different proteins were exclusively found depending on the presence or absence of PICF7 and only one protein with hydrogen ion transmembrane transporter activity was exclusively found in both PICF7-inoculated barley and wheat plants but not in the controls.
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http://dx.doi.org/10.1093/femsec/fiw092DOI Listing
August 2016

Systemic responses in a tolerant olive (Olea europaea L.) cultivar upon root colonization by the vascular pathogen Verticillium dahliae.

Front Microbiol 2015 16;6:928. Epub 2015 Sep 16.

Department of Crop Protection, Institute for Sustainable Agriculture, Consejo Superior de Investigaciones Científicas Córdoba, Spain.

Verticillium wilt of olive (VWO) is caused by the vascular pathogen Verticillium dahliae. One of the best VWO management measures is the use of tolerant cultivars; however, our knowledge on VWO tolerance/resistance genetics is very limited. A transcriptomic analysis was conducted to (i) identify systemic defense responses induced/repressed in aerial tissues of the tolerant cultivar Frantoio upon root colonization by V. dahliae, and (ii) determine the expression pattern of selected defense genes in olive cultivars showing differential susceptibility to VWO. Two suppression subtractive hybridization cDNA libraries, enriched in up-regulated (FU) and down-regulated (FD) genes respectively, were generated from "Frantoio" aerial tissues. Results showed that broad systemic transcriptomic changes are taking place during V. dahliae-"Frantoio" interaction. A total of 585 FU and 381 FD unigenes were identified, many of them involved in defense response to (a)biotic stresses. Selected genes were then used to validate libraries and evaluate their temporal expression pattern in "Frantoio." Four defense genes were analyzed in cultivars Changlot Real (tolerant) and Picual (susceptible). An association between GRAS1 and DRR2 gene expression patterns and susceptibility to VWO was observed, suggesting that these transcripts could be further evaluated as markers of the tolerance level of olive cultivars to V. dahliae.
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http://dx.doi.org/10.3389/fmicb.2015.00928DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4584997PMC
October 2015

Arabidopsis thaliana as a tool to identify traits involved in Verticillium dahliae biocontrol by the olive root endophyte Pseudomonas fluorescens PICF7.

Front Microbiol 2015 7;6:266. Epub 2015 Apr 7.

Department of Crop Protection, Institute for Sustainable Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas, Córdoba Spain.

The effective management of Verticillium wilts (VW), diseases affecting many crops and caused by some species of the soil-borne fungus Verticillium, is problematic. The use of microbial antagonists to control these pathologies fits modern sustainable agriculture criteria. Pseudomonas fluorescens PICF7 is an endophytic bacterium isolated from olive roots with demonstrated ability to control VW of olive caused by the highly virulent, defoliating (D) pathotype of Verticillium dahliae Kleb. However, the study of the PICF7-V. dahliae-olive tripartite interaction poses difficulties because of the inherent characteristics of woody, long-living plants. To overcome these problems we explored the use of the model plant Arabidopsis thaliana. Results obtained in this study showed that: (i) olive D and non-defoliating V. dahliae pathotypes produce differential disease severity in A. thaliana plants; (ii) strain PICF7 is able to colonize and persist in the A. thaliana rhizosphere but is not endophytic in Arabidopsis; and (iii) strain PICF7 controls VW in Arabidopsis. Additionally, as previously observed in olive, neither swimming motility nor siderophore production by PICF7 are required for VW control in A. thaliana, whilst cysteine auxotrophy decreased the effectiveness of PICF7. Moreover, when applied to the roots PICF7 controlled Botrytis cinerea infection in the leaves of Arabidopsis, suggesting that this strain is able to induce systemic resistance. A. thaliana is therefore a suitable alternative to olive bioassays to unravel biocontrol traits involved in biological control of V. dahliae by P. fluorescens PICF7.
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http://dx.doi.org/10.3389/fmicb.2015.00266DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4387922PMC
April 2015

Complete genome sequence of Pseudomonas fluorescens strain PICF7, an indigenous root endophyte from olive (Olea europaea L.) and effective biocontrol agent against Verticillium dahliae.

Stand Genomic Sci 2015 6;10:10. Epub 2015 Feb 6.

Departmentos de Potección de Cultivos y, Campus 'Alameda del Obispo' s/n, Apartado 4084, 14080 Córdoba, Spain.

Pseudomonas fluorescens strain PICF7 is a native endophyte of olive roots. Previous studies have shown this motile, Gram-negative, non-sporulating bacterium is an effective biocontrol agent against the soil-borne fungus Verticillium dahliae, the causal agent of one of the most devastating diseases for olive (Olea europaea L.) cultivation. Here, we announce and describe the complete genome sequence of Pseudomonas fluorescens strain PICF7 consisting of a circular chromosome of 6,136,735 bp that encodes 5,567 protein-coding genes and 88 RNA-only encoding genes. Genome analysis revealed genes predicting factors such as secretion systems, siderophores, detoxifying compounds or volatile components. Further analysis of the genome sequence of PICF7 will help in gaining insights into biocontrol and endophytism.
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http://dx.doi.org/10.1186/1944-3277-10-10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4322347PMC
February 2015

Endophytic colonization and biocontrol performance of Pseudomonas fluorescens PICF7 in olive (Olea europaea L.) are determined neither by pyoverdine production nor swimming motility.

Environ Microbiol 2015 Sep 11;17(9):3139-53. Epub 2015 Feb 11.

Department of Crop Protection, Institute for Sustainable Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC), Alameda del Obispo s/n, Apartado 4084, E-14080, Córdoba, Spain.

Pseudomonas fluorescens PICF7 is an indigenous inhabitant of olive (Olea europaea L.) rhizosphere, able to display endophytic lifestyle in roots, to induce a wide range of defence responses upon colonization of this organ and to exert effective biological control against Verticillium wilt of olive (VWO) (Verticillium dahliae). We aimed to evaluate the involvement of specific PICF7 phenotypes in olive root colonization and VWO biocontrol effectiveness by generating mutants impaired in swimming motility (fliI) or siderophore pyoverdine production (pvdI). Besides, the performance of mutants with diminished in vitro growth in potato dextrose agar medium (gltA) and cysteine (Cys) auxotrophy was also assessed. Results showed that olive root colonization and VWO biocontrol ability of the fliI, pvdI and gltA mutants did not significantly differ from that displayed by the parental strain PICF7. Consequently, altered in vitro growth, swimming motility and pyoverdine production contribute neither to PICF7 VWO suppressive effect nor to its colonization ability. In contrast, the Cys auxotroph mutant showed reduced olive root colonization capacity and lost full biocontrol efficacy. Moreover, confocal laser scanning microscopy revealed that all mutants tested were able to endophytically colonize root tissue to the same extent as wild-type PICF7, discarding these traits as relevant for its endophytic lifestyle.
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http://dx.doi.org/10.1111/1462-2920.12725DOI Listing
September 2015

Early and delayed long-term transcriptional changes and short-term transient responses during cold acclimation in olive leaves.

DNA Res 2015 Feb 16;22(1):1-11. Epub 2014 Oct 16.

Departamento de Biología Experimental, Universidad de Jaén, Jaén, Spain

Low temperature severely affects plant growth and development. To overcome this constraint, several plant species from regions having a cool season have evolved an adaptive response, called cold acclimation. We have studied this response in olive tree (Olea europaea L.) cv. Picual. Biochemical stress markers and cold-stress symptoms were detected after the first 24 h as sagging leaves. After 5 days, the plants were found to have completely recovered. Control and cold-stressed plants were sequenced by Illumina HiSeq 1000 paired-end technique. We also assembled a new olive transcriptome comprising 157,799 unigenes and found 6,309 unigenes differentially expressed in response to cold. Three types of response that led to cold acclimation were found: short-term transient response, early long-term response, and late long-term response. These subsets of unigenes were related to different biological processes. Early responses involved many cold-stress-responsive genes coding for, among many other things, C-repeat binding factor transcription factors, fatty acid desaturases, wax synthesis, and oligosaccharide metabolism. After long-term exposure to cold, a large proportion of gene down-regulation was found, including photosynthesis and plant growth genes. Up-regulated genes after long-term cold exposure were related to organelle fusion, nucleus organization, and DNA integration, including retrotransposons.
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http://dx.doi.org/10.1093/dnares/dsu033DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4379972PMC
February 2015

The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots.

Front Microbiol 2014 5;5:427. Epub 2014 Sep 5.

Lab Plant-Microbe Interactions, Department of Crop Protection, Institute for Sustainable Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC) Córdoba, Spain.

Pseudomonas fluorescens PICF7, a native olive root endophyte and effective biocontrol agent (BCA) against Verticillium wilt of olive, is able to trigger a broad range of defense responses in root tissues of this woody plant. In order to elucidate whether strain PICF7 also induces systemic defense responses in above-ground organs, aerial tissues of olive plants grown under non-gnotobiotic conditions were collected at different time points after root bacterization with this endophytic BCA. A suppression subtractive hybridization (SSH) cDNA library, enriched in up-regulated genes, was generated. This strategy enabled the identification of 376 ESTs (99 contigs and 277 singlets), many of them related to response to different stresses. Five ESTs, involved in defense responses, were selected to carry out time-course quantitative real-time PCR (qRT-PCR) experiments aiming to: (1) validate the induction of these genes, and (2) shed light on their expression pattern along time (from 1 to 15 days). Induction of olive genes potentially coding for lipoxygenase 2, catalase, 1-aminocyclopropane-1-carboxylate oxidase, and phenylananine ammonia-lyase was thus confirmed at some time points. Computational analysis also revealed that different transcription factors were up-regulated in olive aerial tissues (i.e., JERF, bHLH, WRKY), as previously reported for roots. Results confirmed that root colonization by this endophytic bacterium does not only trigger defense responses in this organ but also mounts a wide array of systemic defense responses in distant tissues (stems, leaves). This sheds light on how olive plants respond to the "non-hostile" colonization by a bacterial endophyte and how induced defense response can contribute to the biocontrol activity of strain PICF7.
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http://dx.doi.org/10.3389/fmicb.2014.00427DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4155815PMC
September 2014

From the root to the stem: interaction between the biocontrol root endophyte Pseudomonas fluorescens PICF7 and the pathogen Pseudomonas savastanoi NCPPB 3335 in olive knots.

Microb Biotechnol 2013 May 20;6(3):275-87. Epub 2013 Feb 20.

Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, Consejo Superior de Investigaciones Científicas-CSIC, Alameda del Obispo s/n, Apartado 4084, E-14080 Córdoba, Spain.

Olive knot disease, caused by Pseudomonas savastanoi pv. savastanoi, is one of the most important biotic constraints for olive cultivation. Pseudomonas fluorescens PICF7, a natural colonizer of olive roots and effective biological control agent (BCA) against Verticillium wilt of olive, was examined as potential BCA against olive knot disease. Bioassays using in vitro-propagated olive plants were carried out to assess whether strain PICF7 controlled knot development either when co-inoculated with the pathogen in stems or when the BCA (in roots) and the pathogen (in stems) were spatially separated. Results showed that PICF7 was able to establish and persist in stem tissues upon artificial inoculation. While PICF7 was not able to suppress disease development, its presence transiently decreased pathogen population size, produced less necrotic tumours, and sharply altered the localization of the pathogen in the hyperplasic tissue, which may pose epidemiological consequences. Confocal laser scanning microscopy combined with fluorescent tagging of bacteria revealed that when PICF7 was absent the pathogen tended to be localized at the knot surface. However, presence of the BCA seemed to confine P. savastanoi at inner regions of the tumours. This approach has also enabled to prove that the pathogen can moved systemically beyond the hypertrophied tissue.
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http://dx.doi.org/10.1111/1751-7915.12036DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3815922PMC
May 2013
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