Skip to main content
Log in

Plant defense factors involved in Olea europaea resistance against Xylella fastidiosa infection

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Olive quick decline syndrome (OQDS) is a dangerous plant disease, caused by the bacterium Xylella fastidiosa, which targets olive (Olea europaea). Since field observations suggested that some olive cultivars (i.e. Leccino) were more resistant to OQDS than others (i.e. Cellina di Nardò), the plant defense strategies adopted by olive to contrast X. fastidiosa infection were investigated. In the present study, ELISA and genetic approaches were used to confirm plant infection, while microbial colonization mechanism and distribution in host plant tissues and reactive oxygen species (ROS) levels were examined by light, scanning electron and confocal microscopy analyses. Spectrophotometric and chromatographic techniques were performed to measure secondary metabolites content and qPCR assay was carried out for monitoring plant gene expression variation. Our analysis showed that X. fastidiosa caused accumulation of ROS in Leccino samples compared to Cellina di Nardò. Moreover, the infection induced the up-regulation of defense-related genes, such as NADPH oxidase, some protein kinases, pathogen plant response factors and metabolic enzymes. We also found that Leccino plants enhanced the production of specific antioxidant and antimicrobial molecules, to fight the pathogen and avoid its spreading into xylem vessels. We provided new information on OQDS resistance mechanism applied by Leccino cultivar. In particular, we evidenced that high concentrations of ROS, switching on plant defence signalling pathways, may represent a key factor in fighting X. fastidiosa infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

HC:

Healthy Cellina di Nardò

HL:

Healthy Leccino

IC:

Infected Cellina di Nardò

IL:

Infected Leccino

ROS:

Reactive oxygen species

OQDS:

Olive quick decline syndrome

References

  • Piano degli Interventi art. 1 c.4 dell’OCDPC 225/2015 –http://cartografia.sit.puglia.it/doc/Piano_operativo_Xylella_approvato%2018_03_2015.pdf

  • Acharya BR, Raina S, Maqbool SB, Jagadeeswaran G, Mosher SL, Appel HM et al (2007) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J 50:488–499

    CAS  PubMed  Google Scholar 

  • Alba V, Montemurro C, Sabetta W, Pasqualone A, Blanco A (2009) SSR-based identification key of cultivars of Olea europaea L. diffused in Southern-Italy. Sci Hortic 23:11–16

    Google Scholar 

  • Almeida RP, Nunney L (2015) How do plant diseases caused by Xylella fastidiosa emerge? Plant Dis 99:1457–1467

    PubMed  Google Scholar 

  • Baccari C, Lindow SE (2011) Assessment of the process of movement of Xylella fastidiosa within susceptible and resistant grape cultivars. Phytopathology 101:77–84

    CAS  PubMed  Google Scholar 

  • Baldi P, La Porta N (2017) Xylella fastidiosa: host range and advance in molecular identification techniques. Front Plant Sci 8:944

    PubMed  PubMed Central  Google Scholar 

  • Bartolini G (2012) OLEA databases. http://www.oleadb.it. Accessed 24 Oct 2018

  • Baù A, Delbianco A, Stancanelli G, Tramontini S (2017) Susceptibility of Olea europaea L. varieties to Xylella fastidiosa subsp. pauca ST53: systematic literature search up to 24 March 2017. EFSA J 15:4772

    Google Scholar 

  • Benzie IF, Strain JJ (1999) Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol 299:15–27

    CAS  PubMed  Google Scholar 

  • Boscia D, Saponari M, Palmisano F, Loconsole G, Martelli GP, Savino VN (2014) Field observations on the behaviour of different olive cultivars in response to Xylella fastidiosa infections. In: International symposium on the European outbreak of Xylella fastidiosa in olive. J Plant Pathol 96:107

  • Boscia D, Altamura G, Ciniero A, Di Carolo M, Dongiovanni C, Fumarola G et al (2017) Resistenza a Xylella fastidiosa in diverse cultivar di olivo. Inf Agrar 11:59

    Google Scholar 

  • Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J, Rayapuram C et al (2015) Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLoS Gen 11:e1005373

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Cardinale M, Luvisi A, Meyer JB, Sabella E, De Bellis L, Cruz AC et al (2018) Specific fluorescence in situ hybridization (FISH) test to highlight colonization of xylem vessels by Xylella fastidiosa in naturally infected olive trees (Olea europaea L.). Front Plant Sci 9:431

    PubMed  PubMed Central  Google Scholar 

  • Cariddi C, Saponari M, Boscia D, De Stradis A, Loconsole G, Nigro F et al (2014) Isolation of a Xylella fastidiosa strain infecting olive and oleander in Apulia, Italy. J Plant Pathol 96:1–5

    Google Scholar 

  • Chang C, Yang M, Wen H, Chern J (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182

    CAS  Google Scholar 

  • Charkowski AO (2016) Opportunistic pathogens of terrestrial plants. In: Hurst C (ed) The Rasputin effect: when commensals and symbionts become parasitic. Advances in Environmental Microbiology, vol 3. Springer, Cham, pp 147–168

    Google Scholar 

  • Chen K, Fan B, Du L, Chen Z (2004) Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis. Plant Mol Biol 56:271–283

    CAS  PubMed  Google Scholar 

  • Choi HK, Iandolino A, Da Silva FG, Cook DR (2013) Water deficit modulates the response of Vitis vinifera to the Pierce’s disease pathogen Xylella fastidiosa. Mol Plant Microbe Interact 26:643–657

    CAS  PubMed  Google Scholar 

  • Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341:746–751

    CAS  PubMed  Google Scholar 

  • De Gara L, De Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction. Plant Physiol Biochem 41:863–870

    Google Scholar 

  • Di Marco G, Gismondi A, Canuti L, Scimeca M, Volpe A, Canini A (2014) Tetracycline accumulates in Iberis sempervirens L. plants through apoplastic transport inducing oxidative stress and growth inhibition. Plant Biol 16:792–800

    PubMed  Google Scholar 

  • Dixon RA, Harrison MJ, Lamb CJ (1994) Early events in the activation of plant defense responses. Annu Rev Phytopathol 32:479–501

    CAS  Google Scholar 

  • Fuoco C, Salvatori ML, Biondo A, Shapira-Schweitzer K, Santoleri S, Antonini S et al (2012) Injectable polyethylene glycol-fibrinogen hydrogel adjuvant improves survival and differentiation of transplanted mesoangioblasts in acute and chronic skeletal-muscle degeneration. Skelet Muscle 2:24

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giampetruzzi A, Chiumenti M, Saponari M, Donvito G, Italiano A, Loconsole G et al (2015) Draft genome sequence of the Xylella fastidiosa CoDiRO strain. Genome Announc 3:e01538-14

    PubMed  PubMed Central  Google Scholar 

  • Giampetruzzi A, Morelli M, Saponari M, Loconsole G, Chiumenti M, Boscia D et al (2016) Transcriptome profiling of two olive cultivars in response to infection by the CoDiRO strain of Xylella fastidiosa subsp. pauca. BMC Genom 17:475

    Google Scholar 

  • Gismondi A, Canini A (2013) Microsatellite analysis of Latial Olea europaea L. cultivars. Plant Biosyst 147:686–691

    Google Scholar 

  • Gismondi A, Canuti L, Grispo M, Canini A (2014) Biochemical composition and antioxidant properties of Lavandula angustifolia Miller essential oil are shielded by propolis against UV radiations. J Photochem Photobiol 90:702–708 (erratum, J Photochem Photobiol 90:1214)

    Google Scholar 

  • Gismondi A, Di Marco G, Canuti L, Canini A (2017) Antiradical activity of phenolic metabolites extracted from grapes of white and red Vitis vinifera L. cultivars. VITIS 56:19–26

    CAS  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hopkins DL (1989) Xylella fastidiosa: xylem-limited bacterial pathogen of plants. Annu Rev Phytopathol 27:271–290

    Google Scholar 

  • Hopkins DL, Purcell AH (2002) Xylella fastidiosa: cause of Pierce’s disease of grapevine and other emergent diseases. Plant Dis 86:1056–1066

    CAS  PubMed  Google Scholar 

  • Impei S, Gismondi A, Canuti L, Canini A (2015) Metabolic and biological profile of autochthonous Vitis vinifera L. ecotypes. Food Funct 6:1526–1538

    CAS  PubMed  Google Scholar 

  • ISTAT (2014) http://www.istat.it/it/files/2014/11/C13.pdf. Accessed 9 Oct 2018

  • ISTAT (2015) http://www.istat.it/it/files/2016/12/14-agricoltura.pdf. Accessed 9 Oct 2018

  • Janse JD, Obradovic A (2010) Xylella fastidiosa: its biology, diagnosis, control and risks. J Plant Pathol 92:35–48

    Google Scholar 

  • Jiménez-Ruiz J, Leyva-Pérez MDLO, Schilirò E, Barroso JB, Bombarely A, Mueller L et al (2017) Transcriptomic analysis of Olea europaea L. roots during the Verticillium dahliae early infection process. Plant Genome 10:1–15

    Google Scholar 

  • Katagiri F, Tsuda K (2010) Understanding the plant immune system. Mol Plant Microbe Interact 23:1531–1536

    CAS  PubMed  Google Scholar 

  • Kraepiel Y, Barny MA (2016) Gram-negative phytopathogenic bacteria, all hemibiotrophs after all? Mol Plant Pathol 17:313–316

    PubMed  PubMed Central  Google Scholar 

  • Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leyva-Pérez MDLO, Jiménez-Ruiz J, Gómez-Lama Cabanás C, Valverde-Corredor A, Barroso JB, Luque F, Mercado-Blanco J (2018) Tolerance of olive (Olea europaea) cv Frantoio to Verticillium dahliae relies on both basal and pathogen-induced differential transcriptomic responses. New Phytol 217:671–686

    PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Loconsole G, Potere O, Boscia D, Altamura G, Djelouah K, Elbeaino T et al (2014) Detection of Xylella fastidiosa in olive trees by molecular and serological methods. J Plant Pathol 96:7–14

    Google Scholar 

  • Lou Z, Wang H, Zhu S, Ma C, Wang Z (2011) Antibacterial activity and mechanism of action of chlorogenic acid. J Food Sci 76:398–403

    Google Scholar 

  • Luvisi A, Aprile A, Sabella E, Vergine M, Nicolì F, Nutricati E, Miceli A, Negro C, de Bellis L (2017) Xylella fastidiosa subsp. pauca (CoDiRO strain) infection in four olive (Olea europaea L.) cultivars: profile of phenolic compounds in leaves and progression of leaf scorch symptoms. Phytopathol Mediterr 56:259–273

    CAS  Google Scholar 

  • Marcelletti S, Scortichini M (2016) Xylella fastidiosa CoDiRO strain associated with the olive quick decline syndrome in southern Italy belongs to a clonal complex of the subspecies pauca that evolved in Central America. Microbiology 162:2087–2098

    CAS  PubMed  Google Scholar 

  • Martelli GP (2016) The current status of the quick decline syndrome of olive in southern Italy. Phytoparasitica 44:1–10

    Google Scholar 

  • Martelli GP, Boscia D, Porcelli F, Saponari M (2015) The olive quick decline syndrome in south-east Italy: a threatening phytosanitary emergency. Eur J Plant Pathol 144:235–243

    Google Scholar 

  • McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79–82

    CAS  PubMed  Google Scholar 

  • Min-Sun K, Joung Soung J, Youg-Sig K, Geum-Sook H (2016) Metabolic response of strawberry (Fragaria x ananassa) leaves to the angular leaf spot bacterium (Xanthomonas fragariae). J Agric Food Chem 64:1889–1898

    Google Scholar 

  • Newman KL, Almeida RPP, Purcell AH, Lindow SE (2003) Use of a green fluorescent strain for analysis of Xylella fastidiosa colonization of Vitis venifera. Appl Environ Microbiol 69:7319–7327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niza B, Coletta-Filho HD, Merfa MV, Takita MA, Souza AA (2015) Differential colonization patterns of Xylella fastidiosa infecting citrus genotypes. Plant Pathol 64:1259–1269

    CAS  Google Scholar 

  • Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266

    PubMed  Google Scholar 

  • Onaga G, Wydra K (2016) Advances in plant tolerance to abiotic stresses. In: Plant genomics. Headquarters Publisher, IntechOpen Editors, London, pp 229–272

    Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    PubMed  PubMed Central  Google Scholar 

  • Peralbo-Molina Á, De Castro MD (2013) Potential of residues from the Mediterranean agriculture and agrifood industry. Trends Food Sci Technol 32:16–24

    CAS  Google Scholar 

  • Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764

    CAS  PubMed  Google Scholar 

  • Pogany M, Von Rad U, Grun S, Dongo A, Pintye A, Simoneau P et al (2009) Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol 151:1459–1475

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pomar F, Novo M, Bernal MA, Merino F, Ros Barcelo A (2004) Changes in stem lignins (monomer composition and crosslinking) and peroxidase are related with the maintenance of leaf photosynthetic integrity during Verticillium wilt in Capsicum annuum. New Phytol 163:111–123

    CAS  PubMed  Google Scholar 

  • Purcell AH (2013) Paradigms: examples from the bacterium Xylella fastidiosa. Annu Rev Phytopathol 51:229–356

    Google Scholar 

  • Purcell AH, Hopkins DL (1996) Fastidious xylem-limited bacterial plant pathogens. Annu Rev Phytopathol 34:131–151

    CAS  PubMed  Google Scholar 

  • Rodrigues CM, de Souza AA, Takita MA, Kishi LT, Machado MA (2013) RNA-Seq analysis of Citrus reticulata in the early stages of Xylella fastidiosa infection reveals auxin-related genes as a defense response. BMC Genom 14:676

    CAS  Google Scholar 

  • Sabella E, Luvisi A, Aprile A, Negro C, Vergine M, Nicolì F et al (2018) Xylella fastidiosa induces differential expression of lignification related-genes and lignin accumulation in tolerant olive trees cv. Leccino. J Plant Physiol 220:60–68

    CAS  PubMed  Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, Luis A (2008) Imaging of reactive oxygen species and nitric oxide in vivo in plant tissues. Methods Enzymol 440:397–409

    CAS  PubMed  Google Scholar 

  • Saponari M, Boscia D, Nigro F, Martelli GP (2013) Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (Southern Italy). J Plant Pathol 95:659–668

    Google Scholar 

  • Scarpari LM, Lambais MR, Silva DS, Carraro DM, Carrer H (2003) Expression of putative pathogenicity-related genes in Xylella fastidiosa grown at low and high cell density conditions in vitro. FEMS Microbiol Lett 222:83–92

    CAS  PubMed  Google Scholar 

  • Schaad NW, Postnikova E, Lacy G, Fatmi M, Chang CJ (2004) Xylella fastidiosa subspecies: X. fastidiosa subsp. fastidiosa subsp. nov., X. fastidiosa subsp. multiplex subsp. nov., and X. fastidiosa subsp. pauca subsp. Syst Appl Microbiol 27:290–300

    CAS  PubMed  Google Scholar 

  • Schuenzel EL, Scally M, Stouthamer R, Nunney L (2005) A multigene phylogenetic study of clonal diversity and divergence in North American strains of the plant pathogen Xylella fastidiosa. Appl Environ Microbiol 71:3832–3839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shanmugam MK, Daia X, Kumara AP, Tana BKH, Sethia G, Bishayeee A (2014) Oleanolic acid and its synthetic derivatives for the prevention and therapy of cancer: preclinical and clinical evidence. Cancer Lett 346:206–216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14

    CAS  Google Scholar 

  • Silva S, Gomes L, Leitao F, Coelho AV, Boas V (2006) Phenolic compounds and antioxidant activity of Olea europaea L. fruits and leaves. Food Sci Technol Int 12:385–396

    CAS  Google Scholar 

  • Simpson AJ, Reinach FC, Arruda P et al (2000) The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406:151–157

    CAS  PubMed  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticult 16:144–158

    CAS  Google Scholar 

  • Su CC, Deng WL, Jan FJ, Chang CJ, Huang H, Shih HT, Chen J (2016) Xylella taiwanensis sp. nov., causing pear leaf scorch disease. Int J Syst Evol Microbiol 66:4766–4771

    CAS  PubMed  Google Scholar 

  • Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522

    CAS  PubMed  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiol 141:373–378

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weir IE, Maddumage R, Allan AC, Ferguson IB (2005) Flow cytometric analysis of tracheary element differentiation in Zinnia elegans cells. Cytometry 68:81–91

    PubMed  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S et al (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:95

    PubMed  PubMed Central  Google Scholar 

  • Yadeta KA, Elmore JM, Creer AY, Feng B, Franco JY, Rufian JS et al (2017) A cysteine-rich protein kinase associates with a membrane immune complex and the cysteine residues are required for cell death. Plant Physiol 173:771–787

    CAS  PubMed  Google Scholar 

  • Yeh YH, Chang YH, Huang PY, Huang JB, Zimmerli L (2015) Enhanced Arabidopsis pattern-triggered immunity by overexpression of cysteine-rich receptor-like kinases. Front. Plant Sci 6:322

    PubMed  PubMed Central  Google Scholar 

  • Yuan X, Morano L, Bromley R, Spring-Pearson S, Stouthamer R, Nunnery L (2010) Multilocus sequence typing of Xylella fastidiosa causing Pierce’s disease and oleander leaf scorch in the United States. Phytopathology 100:601–611

    CAS  PubMed  Google Scholar 

  • Zhang J, Shao F, Li Y, Cui H, Chen L, Lin H et al (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Daniele Giaffreda for his work as intermediary with Agricultural Farms, the Agricultural Farm of Ing. Niccolò Coppola-srl-S.S. 101, Km 34.5-Tenuta di Torre Sabea 73014 Gallipoli (LE) and the Agricultural Farm of Cosimo Tornesello-Contrada Monaci Gallipoli-73048 (LE) which kindly provided olive samples, the Advanced Microscopies Center (AMC) of the University of Rome “Tor Vergata”, Biology Department, Dr. Elena Romano for her technical expertise in confocal microscopy analysis and Dr. Francesco Basoli for his contribution in SEM analysis A deep gratitude to “Ministero delle Politiche Agricole, Alimentari e Forestali, ex. DG Sviluppo Rurale, ex. DISR V-Produzioni vegetali”, “Regione Puglia-Area Politiche per lo Sviluppo Rurale, Servizio Agricoltura, Ufficio Osservatorio Fitosanitario” and “Regione Lazio-Direzione Regionale Agricoltura, Servizio Fitosanitario Regionale, Innovazione in Agricoltura” for authorisation to collect samples and work on this topic (DG DISR-DISR 05-Prot. Uscita N. 0023466 del 03/10/2016).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antonella Canini.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 825 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Novelli, S., Gismondi, A., Di Marco, G. et al. Plant defense factors involved in Olea europaea resistance against Xylella fastidiosa infection. J Plant Res 132, 439–455 (2019). https://doi.org/10.1007/s10265-019-01108-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-019-01108-8

Keywords

Navigation