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Comparative Genomics of Pathogenic and Nonpathogenic Strains Of Comparative Genomics of Pathogenic and Nonpathogenic Strains of Xanthomonas arboricola Unveil Molecular and Evolutionary Events Linked to Pathoadaptation Sophie Cesbron, Martial Briand, Salwa Es-Sakhi, Sophie Gironde, Tristan Boureau, Charles Manceau, Marion Le Saux, Marie Agnes Jacques To cite this version: Sophie Cesbron, Martial Briand, Salwa Es-Sakhi, Sophie Gironde, Tristan Boureau, et al.. Compara- tive Genomics of Pathogenic and Nonpathogenic Strains of Xanthomonas arboricola Unveil Molecular and Evolutionary Events Linked to Pathoadaptation. Frontiers in Plant Science, Frontiers, 2015, 6 (article 1126), 19 p. 10.3389/fpls.2015.01126. hal-01455982 HAL Id: hal-01455982 https://hal.archives-ouvertes.fr/hal-01455982 Submitted on 27 May 2020 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. ORIGINAL RESEARCH published: 22 December 2015 doi: 10.3389/fpls.2015.01126 Comparative Genomics of Pathogenic and Nonpathogenic Edited by: Thomas Lahaye, Strains of Xanthomonas arboricola Ludwig-Maximilians-University Munich, Germany Unveil Molecular and Evolutionary Reviewed by: Liliana Maria Cano, North Carolina State University, USA Events Linked to Pathoadaptation Matthew James Moscou, The Sainsbury Laboratory, UK Sophie Cesbron 1*, Martial Briand 1, Salwa Essakhi 1 †, Sophie Gironde 1 †, Tristan Boureau 2, 1 † 1‡ 1‡ *Correspondence: Charles Manceau , Marion Fischer-Le Saux and Marie-Agnès Jacques Sophie Cesbron 1 INRA, UMR 1345 Institut de Recherche en Horticulture et Semences, Beaucouzé, France, 2 Université d’Angers, UMR 1345 [email protected] Institut de Recherche en Horticulture et Semences, Angers, France †Present Address: Salwa Essakhi, GDEC - Genetics, Diversity The bacterial species Xanthomonas arboricola contains plant pathogenic and Ecophysiology of Cereals INRA, UMR nonpathogenic strains. It includes the pathogen X. arboricola pv. juglandis, causing 1095, Lempdes, France; Sophie Gironde, the bacterial blight of Juglans regia. The emergence of a new bacterial disease of Terrena, Ancenis, France; J. regia in France called vertical oozing canker (VOC) was previously described and the Charles Manceau, causal agent was identified as a distinct genetic lineage within the pathovar juglandis. ANSES - French Agency for Food, Environmental and Occupational Symptoms on walnut leaves and fruits are similar to those of a bacterial blight but Health & Safety, Plant Health VOC includes also cankers on trunk and branches. In this work, we used comparative Laboratory, Angers, France genomics and physiological tests to detect differences between four X. arboricola strains ‡These authors have contributed equally to this work. isolated from walnut tree: strain CFBP 2528 causing walnut blight (WB), strain CFBP 7179 causing VOC and two nonpathogenic strains, CFBP 7634 and CFBP 7651, Specialty section: isolated from healthy walnut buds. Whole genome sequence comparisons revealed This article was submitted to Plant Biotic Interactions, that pathogenic strains possess a larger and wider range of mobile genetic elements a section of the journal than nonpathogenic strains. One pathogenic strain, CFBP 7179, possessed a specific Frontiers in Plant Science integrative and conjugative element (ICE) of 95 kb encoding genes involved in copper Received: 29 May 2015 resistance, transport and regulation. The type three effector repertoire was larger in Accepted: 27 November 2015 Published: 22 December 2015 pathogenic strains than in nonpathogenic strains. Moreover, CFBP 7634 strain lacked the Citation: type three secretion system encoding genes. The flagellar system appeared incomplete Cesbron S, Briand M, Essakhi S, and nonfunctional in the pathogenic strain CFBP 2528. Differential sets of chemoreceptor Gironde S, Boureau T, Manceau C, and different repertoires of genes coding adhesins were identified between pathogenic Fischer-Le Saux M and Jacques M-A (2015) Comparative Genomics of and nonpathogenic strains. Besides these differences, some strain-specific differences Pathogenic and Nonpathogenic were also observed. Altogether, this study provides valuable insights to highlight the Strains of Xanthomonas arboricola Unveil Molecular and Evolutionary mechanisms involved in ecology, environment perception, plant adhesion and interaction, Events Linked to Pathoadaptation. leading to the emergence of new strains in a dynamic environment. Front. Plant Sci. 6:1126. doi: 10.3389/fpls.2015.01126 Keywords: Juglans regia, vertical oozing canker, bacterial blight, ICE, copper resistance Frontiers in Plant Science | www.frontiersin.org 1 December 2015 | Volume 6 | Article 1126 Cesbron et al. Comparative Genomics of X. arboricola INTRODUCTION In this report, we present genomic comparisons of four X. arboricola strains isolated from walnut tree that are Xanthomonads are bacteria associated to plants and are representative of the bacterial diversity encountered on J. regia commonly pathogens of plants (Vauterin et al., 2000). These and that were previously analyzed by MLSA, MLVA, and T3Es bacteria can infect a wide host range and cause diseases on more repertoire (Hajri et al., 2012; Essakhi et al., 2015; Fischer- than 124 monocot species and 268 dicot species including cereals, Le Saux et al., 2015). Strain CFBP 2528 (the type strain solanaceous and brassicaceous plants, stone and nut fruit trees of the species), which causes WB, strain CFBP 7179, which (Hayward, 1993; Vauterin et al., 2000). Symptoms and plant parts causes VOC, both included in the pathovar juglandis and two affected are diverse, however each strain is characterized by a nonpathogenic strains, CFBP 7651 and CFBP 7634, isolated from narrow host range. This has led to the definition of the pathovar healthy walnut buds and representing two genetic lineages of concept. A pathovar is a group of strains responsible for the same nonpathogenic strains with and without hrp/hrc genes coding disease on the same host range (Dye et al., 1980). the T3SS respectively were chosen (Essakhi et al., 2015). The X. arboricola comprises pathogenic strains distributed in aim of this work is to identify differences between pathogenic different pathovars (Fischer-Le Saux et al., 2015). The most and nonpathogenic strains, in order to unveil mechanisms of economically important pathovars in X. arboricola are pathovars emergence of pathogenic strains. Based on genomic results, pruni, corylina, and juglandis, which affect stone and nut fruit phenotypic tests were conducted in an attempt to link genomic trees. X. arboricola pv juglandis is the causal agent of walnut content to phenotypic features. blight (WB), a serious disease of Persian (English) walnut. It causes necrosis on leaves, catkins, twigs, and fruits, and can induce important crop losses. A few years ago, a new genetic MATERIALS AND METHODS lineage was identified within X. arboricola pv juglandis as the causal agent of a new disease called vertical oozing canker (VOC) Bacterial Strains (Hajri et al., 2010). Nonpathogenic X. arboricola strains were Bacterial strains used in this study are listed in Table S1. Strains also isolated from walnut tree during surveys of French orchards. of X. arboricola were obtained from the International Center These strains are unable to cause any disease on walnut tree and for Microbial Resources, French Collection for Plant-associated other plant species (Essakhi et al., 2015). Such xanthomonads, Bacteria, (CIRM-CFBP), INRA, Angers, France (http://www. nonpathogenic strains on their host of isolation, have already angers.inra.fr/cfbp/) or isolated from buds of healthy walnuts been isolated from a range of different plants (Vauterin et al., in the two main walnut-growing areas in France (Rhône-Alpes region in the southeast and Périgord in the southwest). Bacterial 1996; Vandroemme et al., 2013a; Triplett et al., 2015). Within ◦ X. arboricola, nonpathogenic strains from Juglans regia and strains were routinely grown at 27 C on TSA medium (3 g/l from Fragaria × ananassa are phylogenetically diverse and do trypton soya broth; 10 g/l agar) for 24–48 h. not cluster according to their host of isolation contrary to pathogenic strains from pathovars pruni, corylina, and juglandis Genomic DNA Isolation, Sequencing, and (Vandroemme et al., 2013a; Essakhi et al., 2015; Fischer-Le Saux Annotation et al., 2015). Genomic DNAs from the strains CFBP 2528, CFBP 7179, CFBP Type three effectors (T3Es) secreted in host plant cells via 7634, and CFBP 7651 were isolated and purified using the the type three secretion system (T3SS) play a basic role in Qiagen’s genome DNA isolation kit (Qiagen, Hilden, Germany) pathogenicity and host specificity of xanthomonads (Hajri et al., according to the manufacturer’s instructions. The Genomic 2009). It was previously shown that strains causing WB and VOC DNA quality and quantity were assessed on an agarose gel and diseases differ by their T3E repertoires, which is composed of using a NanoDrop ND-1000 spectrophotometer (the NanoDrop 17 T3Es (Hajri et al., 2012). The strains causing VOC could be Technologies, Wilmington, DE). Libraries
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