Transcriptome profiling of two olive cultivars in response to infection by the CoDiRO strain of Xylella fastidiosa subsp. pauca

Giampetruzzi et al. BMC Genomics (2016) 17:475 DOI 10.1186/s12864-016-2833-9 RESEARCH ARTICLE Open Access Transcriptome profiling of two olive cultivars in response to infection by the CoDiRO strain of Xylella fastidiosa subsp. pauca Annalisa Giampetruzzi1, Massimiliano Morelli2, Maria Saponari2, Giuliana Loconsole1, Michela Chiumenti2, Donato Boscia2, Vito N. Savino1, Giovanni P. Martelli1 and Pasquale Saldarelli2* Abstract Background: The recent Xylella fastidiosa subsp. pauca (Xfp) outbreak in olive (Olea europaea) groves in southern Italy is causing a destructive disease denoted Olive Quick Decline Syndrome (OQDS). Field observations disclosed that Xfp-infected plants of cv. Leccino show much milder symptoms, than the more widely grown and highly susceptible cv. Ogliarola salentina. To determine whether these field observations underlie a tolerant condition of cv. Leccino, which could be exploited for lessening the economic impact of the disease on the local olive industry, transcriptional changes occurring in plants of the two cultivars affected by Xfp were investigated. Results: A global quantitative transcriptome profiling comparing susceptible (Ogliarola salentina) and tolerant (Leccino) olive cultivars, infected or not by Xfp, was done on messenger RNA (mRNAs) extracted from xylem tissues. The study revealed that 659 and 447 genes were differentially regulated in cvs Leccino and Ogliarola upon Xfp infection, respectively, whereas 512 genes were altered when the transcriptome of both infected cultivars was compared. Analysis of these differentially expressed genes (DEGs) shows that the presence of Xfp is perceived by the plants of both cultivars, in which it triggers a differential response strongly involving the cell wall. Up-regulation of genes encoding receptor-like kinases (RLK) and receptor-like proteins (RLP) is the predominant response of cv. Leccino, which is missing in cv. Ogliarola salentina. Moreover, both cultivars react with a strong re-modelling of cell wall proteins. These data suggest that Xfp elicits a different transcriptome response in the two cultivars, which determines a lower pathogen concentration in cv. Leccino and indicates that this cultivar may harbor genetic constituents and/or regulatory elements which counteract Xfp infection. Conclusions: Collectively these findings suggest that cv. Leccino is endowed with an intrinsic tolerance to Xfp, which makes it eligible for further studies aiming at investigating molecular basis and pathways modulating its different defense response. Keywords: Xylella, de novo assembly, Transcriptome, Olive, xylem, Tolerance, Differentially expressed genes, LRR, RLK, ABA * Correspondence: 2 Consiglio Nazionale delle Ricerche, Istituto per la Protezione Sostenibile delle Piante, SS Bari, via Amendola 122/D, Bari, Italy Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Giampetruzzi et al. BMC Genomics (2016) 17:475 Background Xylella fastidiosa (Xf ) is a polyphagous bacterium causing important diseases of a wide number of crops [1, 2], to which olive (Olea europaea) has recently been added. In this last species a strain of Xf subsp. pauca (Xfp) denoted CoDiRO (abbreviation from the Italian “Complesso del Disseccamento Rapido dell’Olivo”) is associated with a destructive disease named Olive Quick Decline Syndrome (OQDS) [3]. Xfp pathogenicity to olive has been recently demonstrated for the CoDiRo strain [4] further underlining the aggressive nature of this bacterium and its potential threat for the Mediterranean and European agriculture. Being olive a new host, knowledge on the Xf-olive pathosystem is lacking, including the aspects concerning the plant response to the pathogen. The final outcome of a Xf infection is strongly influenced by the association that the bacterium establishes with the host plant, which could range from commensalism to pathogenicity. Indeed, in several species, Xf multiplies and colonizes the host without inducing symptoms, whereas in other, a classical leaf scorching recalling water deficit occurs. Hypotheses behind these symptoms rely on the occlusion of xylem vessels by bacterial colonies aggregated in a biofilm envelope and a plant defense response consisting in the production of tyloses and gums. This speciesconditioned behavior, which likely depends on host physiology and/or response to the infection and on the peculiar Xf subspecies, is also reflected by the lack of virulence genes and effector proteins, which are present in the genome of other bacterial pathogens, like those encoding the type III secretion system. Because of all the above the current view retains that a disease occurs when the bacterium spreads and multiplies exceeding a certain threshold level and/or finds physiological conditions that make it shifting from a commensalistic relationship to disease induction [5] A key question regarding Xf-plant interactions is to understand whether and how the host perceives a pathogen that colonizes the xylem, a tissue mainly composed, in its ultimate developmental stage, of dead cells. Choi et al. [5] demonstrated that xylem-associated cells, particularly those belonging to the protoxylem, sense the presence of the bacterium or of host molecules, i.e. cellwall degradation products originating from cell wall degrading enzymes (CWDEs) secreted by the pathogen. These authors propose a model in which Xf-infected grapevines affected by Pierce's disease specifically perceive the pathogen and respond to its presence by an abscissic acid (ABA)-mediated management of the drought stress imposed by the bacterium. Paradoxically, being ABA a negative regulator of the plant immune response, the possible host defense response is neutralized, thus provoking the establishment of the disease. Page 2 of 18 In a similar study, aimed at disclosing Citrus reticulata resistance to Xf [6] by transcriptome profiling, a clear response to the infection was detected, as triggered by the perception of the bacterium, that elicited cell wall remodelling and up-regulation of different hormones (auxin, ABA and jasmonic acid). In both studies common defense mechanisms were identified consisting on the up-regulation of pattern recognition receptors (PRRs) and the perturbation of cell wall architectural modification and enzymes necessary for biosynthesis of its constituents. Inde (...truncated)