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      Molecular Typing Reveals High Genetic Diversity of Xanthomonas translucens Strains Infecting Small-Grain Cereals in Iran

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          Abstract

          Bacterial leaf streak (BLS) of small-grain cereals (i.e., wheat and barley) is one of the economically important diseases of gramineous crops worldwide. The disease occurs in many countries across the globe, with particular importance in regions characterized by high levels of precipitation. Two genetically distinct xanthomonads—namely, Xanthomonas translucens pv. undulosa and X. translucens pv. translucens—have been reported to cause BLS disease on small-grain cereals. As seed-borne pathogens, the causal agents are included in the A2 list of quarantine pathogens by the European and Mediterranean Plant Protection Organization (EPPO). Despite its global distribution and high economic importance, the population structure, genetic diversity, and phylogeography of X. translucens remain undetermined. This study, using MLSA and MLST, provides a global-scale phylogeography of X. translucens strains infecting small-grain cereals. Based on the diversity parameters, neutrality indices, and population structure, we observe higher genetic diversity of the BLS pathogen in Iran, which is geographically close to the center of origin of common wheat, than has so far been observed in other areas of the world, including North America. The results obtained in this study provide a novel insight into the genetic diversity and population structure of the BLS pathogen of small-grain cereals on a global scale.

          ABSTRACT

          This study provides a phylogeographic insight into the population diversity of Xanthomonas translucens strains causing bacterial leaf streak disease of small-grain cereals in Iran. Among the 65 bacterial strains isolated from wheat, barley, and gramineous weeds in eight Iranian provinces, multilocus sequence analysis and typing (MLSA and MLST) of four housekeeping genes ( dnaK, fyuA, gyrB, and rpoD), identified 57 strains as X. translucens pv. undulosa, while eight strains were identified as X. translucens pv. translucens. Although the pathogenicity patterns on oat and ryegrass weed species varied among the strains, all X. translucens pv. undulosa strains were pathogenic on barley, Harding’s grass, rye (except for XtKm35) and wheat, and all X. translucens pv. translucens strains were pathogenic on barley and Harding’s grass, while none of the latter group was pathogenic on rye or wheat (except for XtKm18). MLST using the 65 strains isolated in Iran, as well as the sequences of the four genes from 112 strains of worldwide origin retrieved from the GenBank database, revealed higher genetic diversity (i.e., haplotype frequency, haplotype diversity, and percentage of polymorphic sites) among the Iranian population of X. translucens than among the North American strains of the pathogen. High genetic diversity of the BLS pathogen in Iran was in congruence with the fact that the Iranian Plateau is considered the center of origin of cultivated wheat. However, further studies using larger collections of strains are warranted to precisely elucidate the global population diversity and center of origin of the pathogen.

          IMPORTANCE Bacterial leaf streak (BLS) of small-grain cereals (i.e., wheat and barley) is one of the economically important diseases of gramineous crops worldwide. The disease occurs in many countries across the globe, with particular importance in regions characterized by high levels of precipitation. Two genetically distinct xanthomonads—namely, Xanthomonas translucens pv. undulosa and X. translucens pv. translucens—have been reported to cause BLS disease on small-grain cereals. As seed-borne pathogens, the causal agents are included in the A2 list of quarantine pathogens by the European and Mediterranean Plant Protection Organization (EPPO). Despite its global distribution and high economic importance, the population structure, genetic diversity, and phylogeography of X. translucens remain undetermined. This study, using MLSA and MLST, provides a global-scale phylogeography of X. translucens strains infecting small-grain cereals. Based on the diversity parameters, neutrality indices, and population structure, we observe higher genetic diversity of the BLS pathogen in Iran, which is geographically close to the center of origin of common wheat, than has so far been observed in other areas of the world, including North America. The results obtained in this study provide a novel insight into the genetic diversity and population structure of the BLS pathogen of small-grain cereals on a global scale.

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          Author and article information

          Contributors
          Role: Editor
          Journal
          Appl Environ Microbiol
          Appl. Environ. Microbiol
          aem
          aem
          AEM
          Applied and Environmental Microbiology
          American Society for Microbiology (1752 N St., N.W., Washington, DC )
          0099-2240
          1098-5336
          16 August 2019
          1 October 2019
          15 October 2019
          : 85
          : 20
          : e01518-19
          Affiliations
          [a ] Department of Plant Protection, College of Agriculture, Shiraz University, Shiraz, Iran
          [b ] Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran
          [c ] State Key Laboratory of Microbial Metabolism, School of Life Science & Biotechnology, Shanghai Jiao Tong University, Shanghai, China
          [d ] Laboratory of Phytopathology-Applied Microbiology, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
          [e ] Interactions Plantes Microorganismes Environnement (IPME), IRD, Cirad, Université de Montpellier, Montpellier, France
          University of Illinois at Chicago
          Author notes
          Address correspondence to Ebrahim Osdaghi, eosdaghi@ 123456shirazu.ac.ir .

          Citation Khojasteh M, Taghavi SM, Khodaygan P, Hamzehzarghani H, Chen G, Bragard C, Koebnik R, Osdaghi E. 2019. Molecular typing reveals high genetic diversity of Xanthomonas translucens strains infecting small-grain cereals in Iran. Appl Environ Microbiol 85:e01518-19. https://doi.org/10.1128/AEM.01518-19.

          Author information
          https://orcid.org/0000-0002-0359-0398
          Article
          PMC6805075 PMC6805075 6805075 01518-19
          10.1128/AEM.01518-19
          6805075
          31420337
          49945012-be34-4819-80f0-cc513b3fd686
          Copyright © 2019 American Society for Microbiology.

          All Rights Reserved.

          History
          : 8 July 2019
          : 6 August 2019
          Page count
          supplementary-material: 1, Figures: 3, Tables: 3, Equations: 0, References: 38, Pages: 15, Words: 9000
          Funding
          Funded by: Shiraz University, https://doi.org/10.13039/501100005071;
          Award ID: PhD grant
          Award Recipient :
          Categories
          Plant Microbiology
          Custom metadata
          October 2019

          bacterial leaf streak, Triticum aestivum ,phylogeography,MLST,MLSA,Iranian Plateau, Hordeum vulgare

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