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Phytoplasma Induces Significant Reprogramming of the Leaf Transcriptome in the Field Grown Grapevine

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Phytoplasma Induces Significant Reprogramming of the Leaf Transcriptome in the Field Grown Grapevine ’Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. Matjaz Hren, Petra Nikolić, Ana Rotter, Andrej Blejec, Nancy Terrier, Maja Ravnikar, Marina Dermastia, Kristina Gruden To cite this version: Matjaz Hren, Petra Nikolić, Ana Rotter, Andrej Blejec, Nancy Terrier, et al.. ’Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine.. BMC Genomics, BioMed Central, 2009, 10, 17 p. 10.1186/1471-2164-10-460. hal-02275509 HAL Id: hal-02275509 https://hal.archives-ouvertes.fr/hal-02275509 Submitted on 30 Aug 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License BMC Genomics BioMed Central Research article Open Access 'Bois noir' phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine Matjaž Hren1, Petra Nikolić1, Ana Rotter1, Andrej Blejec1, Nancy Terrier2, Maja Ravnikar1, Marina Dermastia*1 and Kristina Gruden1 Address: 1National Institute of Biology, Department of Biotechnology and Systems Biology, Večna pot 111, 1000 Ljubljana, Slovenia and 2UMR SPO, Campus Agro-M/INRA, 2 Place Viala, 34060 Montpellier, Cedex 01, France Email: Matjaž Hren - [email protected]; Petra Nikolić - [email protected]; Ana Rotter - [email protected]; Andrej Blejec - [email protected]; Nancy Terrier - [email protected]; Maja Ravnikar - [email protected]; Marina Dermastia* - [email protected]; Kristina Gruden - [email protected] * Corresponding author Published: 2 October 2009 Received: 18 March 2009 Accepted: 2 October 2009 BMC Genomics 2009, 10:460 doi:10.1186/1471-2164-10-460 This article is available from: http://www.biomedcentral.com/1471-2164/10/460 © 2009 Hren et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Phytoplasmas are bacteria without cell walls from the class Mollicutes. They are obligate intracellular plant pathogens which cause diseases in hundreds of economically important plants including the grapevine (Vitis vinifera). Knowledge of their biology and the mechanisms of their interactions with hosts is largely unknown because they are uncultivable and experimentally inaccessible in their hosts. We detail here the global transcriptional profiling in grapevine responses to phytoplasmas. The gene expression patterns were followed in leaf midribs of grapevine cv. 'Chardonnay' naturally infected with a phytoplasma from the stolbur group 16SrXII- A, which is associated with the grapevine yellows disease 'Bois noir'. Results: We established an on field experimental system in a productive vineyard that allowed application of molecular tools in a plant natural environment. Global transcription profiles of infected samples were compared with the healthy ones using microarray datasets and metabolic pathway analysis software (MapMan). The two- year-long experiment revealed that plant genes involved in primary and secondary metabolic pathways were changed in response to infection and that these changes might support phytoplasma nutrition. A hypothesis that phytoplasmas interact with the plant carbohydrate metabolism was proven and some possibilities how the products of this pathway might be utilized by phytoplasmas are discussed. In addition, several photosynthetic genes were largely down-regulated in infected plants, whereas defense genes from the metabolic pathway leading to formation of flavonoids and some PR proteins were significantly induced. Few other genes involved in defense- signaling were differentially expressed in healthy and infected plants. A set of 17 selected genes from several differentially expressed pathways was additionally analyzed with quantitative real-time PCR and confirmed to be suitable for a reliable classification of infected plants and for the characterization of susceptibility features in the field conditions. Conclusion: This study revealed some fundamental aspects of grapevine interactions with the stolbur 'Bois noir' phytoplasma in particular and some plant interactions with phytoplasmas in general. In addition, the results of the study will likely have an impact on grape improvement by yielding marker genes that can be used in new diagnostic assays for phytoplasmas or by identifying candidate genes that contribute to the improved properties of grape. Page 1 of 17 (page number not for citation purposes) BMC Genomics 2009, 10:460 http://www.biomedcentral.com/1471-2164/10/460 Background vine growing countries worldwide. Several molecularly Phytoplasmas are plant pathogenic bacteria belonging to distinct phytoplasma groups which cause the GY were the class Mollicutes [1]. They are cell wall-free, and both identified; however, a phytoplasma from the stolbur their cell size (0.1-0.8 μm in diameter) and genome size group/16SrXII-A [3], associated with the GY disease 'Bois (0.5-1.3 Mbp) are the smallest among bacteria. They are noir', is very common. The name for this phytoplasma transmitted from plant to plant by sap-feeding insect vec- 'Ca. P. solani' has been proposed at the X International tors and they propagate within the cytoplasm of both Congress of the International Organization of Mycoplas- insects and plants. In plants they exclusively inhabit nutri- mology (1994), but the phytoplasma has not been for- ent-rich phloem tissues, where they have been docu- mally described yet. Accordingly it is referred to as 'Bois mented by electron microscopy in sieve elements, noir' ('BN') phytoplasma. Typical symptoms of all phyto- companion cells and phloem parenchyma cells [2]. Phy- plasma infection in grapevine are leaf curling and discol- toplasmas have a broad range of plant hosts among oration of leaf veins and laminas, interveinal yellowing or monocots and dicots and diseases of many important reddening, according to the variety, uneven or total lack of crops have already been associated with these pathogens lignification of canes, flower abortion and berry wither- [1]. Since the discovery of phytoplasmas four decades ago, ing. Leaves on the affected shoots often have a hard, brittle attempts to culture them in cell-free media have failed, texture. making it difficult to determine the taxonomic status of phytoplasmas by the traditional methods applied to cul- In order to demonstrate the potential of grapevine plants tured prokaryotes. Although satisfaction of Koch postu- infected with 'BN' phytoplasma to interact with their lates has not yet been achieved, in order to start formal pathogen, we present here the qualitative and quantitative classification of phytoplasmas the 'Candidatus Phyto- changes in the global gene expression profiles of the plasma' genus has been proposed and adopted [3]. How- healthy and infected plants of cv. 'Chardonnay'. The ever, some phytoplasmas have had an informal experiment was carried out in a production vineyard over description, but they have not been validly described. For two successive growing seasons. Whereas studies of plant them the practice of naming a phytoplasma on the basis responses to pathogen infection conducted under control- of the associated plant syndrome is still valid [3]. led laboratory or glasshouse conditions can focus on the impact of individual factors, it is the resulting changes in Recent progress in the sequencing of four phytoplasma the transcript profile of the field established system that genomes and their comparative analysis [4-7] have potentially uncovers the complexity of signaling networks increased our understanding of phytoplasma genetics and involved in the pathogenicity [11]. A complementary revealed that these plant pathogens experienced substan- experimental system for analyzing gene expression profil- tial evolutionary gene decay, gene loss, and disruption or ing in the field grown 'BN' phytoplasma infected grape- loss of important biosynthetic pathways [8]. These vine has been described very recently [12]. The present genomic changes may account for their complete reliance work is an extension of our recent study on three genes on the host plant or insect cells for survival. encoding sucrose synthase, alcohol dehydrogenase 1 and Hsp70 that are differentially expressed in different grape- As no phytoplasma cultures are available, not all the vine cultivars infected with phytoplasmas [13], to a high approaches can be applied and studies on phytoplasma throughput transcriptome analysis of the infected cv. interactions with host plants are limited. However, the lat- 'Chardonnay'. We analyzed the traits of infection and fur- ter have been mostly studied in periwinkle (Cataranthus ther evaluated the potential contribution of several meta- roseus). Phytoplasmas can be transmitted to periwinkle via bolic/signaling host pathways
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