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Pathogenicity, host range and phylogenetic position of Agrobacterium species associated with sugar beet crown gall outbreaks in Southern Iran

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Abstract

In autumn 2013, an alert concerning a suspected outbreak of sugar beet disease under field conditions has received from Eghlid county, Fars province, Southern Iran. Field surveys were performed following the alert and plants affected with crown gall and tuber deformation were observed. Diseased plants were randomly collected and brought to the laboratory for the isolation and characterization of the causal agent through biochemical, pathogenicity and host range tests under greenhouse conditions on seven crop, ornamental and weed species including carrot, sunflower, and tomato, Christmas kalanchoe and rose ornamentals, and rough milk thistle weed, in addition to sugar beet. Further, sugar content of both infected and non-infected plants was determined. Based on biochemical and molecular tests, the causal agents were identified as members of the Agrobacterium tumefaciens species complex. In pathogenicity and host range tests, all bacterial strains induced lateral and globular galls on the plant species tested. Phylogenetic analysis using the sequences of gyrB housekeeping gene revealed that A. tumefaciens strains isolated from sugar beet belonged to the biovar 1 species complex but divided into two different genomo-species (G3 and G7). No phylogenetic similarities were found among the A. tumefaciens species complex strains isolated from fig, peach, rose, and sugar beet in Iran. The sugar content analysis showed 3 % reduction in sugar content of the infected tubers compared to the healthy ones, which resulted in 24 % reduction in the tubers’ price. Our study reports the outbreaks of an economically important disease, which may further spread and affect the sugar beet industry in Southern Iran.

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References

  • Abdollahian-Noghabi, M., Sharifi, H., Babaei, B., & Bahmani, G., A. (2014). Introduction of a new formula for determination of autumn sugar beet purchase price. Journal of Sugar Beet, 29, 115–121. doi:10.1515/cerce-2015-0013.

  • Anonymous (2014). Agricultural Statistics, Vol. 1. 2012–2013 Cropping Seasons. Ministry of Jihad-e-Agriculture, Tehran, Iran (in Persian), 156p.

  • Aysan, Y., & Sahin, F. (2003). An outbreak of crown gall disease on rose caused by Agrobacterium tumefaciens in Turkey. New Disease Reports, 7, 2.

    Google Scholar 

  • Bini, F., Kuczmog, A., Putnoky, P., Otten, L., Bazzi, C., & Szegedi, E. (2008). Novel pathogen-specific primers for the detection of Agrobacterium vitis and Agrobacterium tumefaciens. Vitis, 47, 181–189.

    CAS  Google Scholar 

  • Carruthers, A., Dutton, J. V., Oldfield, J. F. T., Shore, M., & Teague, H. J. (1960). Juice composition in relation to factory performance. Paper presented to the 13th Annual Technical Conference, British Sugar Corporation Ltd.

  • Costechareyre, D., Rhouma, A., Lavire, C., Portier, P., Chapulliot, D., Bertolla, F., Boubaker, A., Dessaux, Y., & Nesme, X. (2010). Rapid and efficient identification of Agrobacterium species by recA allele analysis: Agrobacterium recA diversity. Microbial Ecology, 60, 862–872. doi:10.1007/s00248-010-9685-7.

    Article  CAS  PubMed  Google Scholar 

  • Farrand, S. K., Van Berkum, P. B., & Oger, P. (2003). Agrobacterium is a definable genus of the family Rhizobiaceae. International Journal of Systematic and Evolutionary Microbiology, 53, 1681–1687.

    Article  CAS  PubMed  Google Scholar 

  • Gouda, M. I., & Emeran, A. A. (2006). First report of sugar beet crown wart disease caused by Urophlyctis leproides in Egypt. New Disease Reports, 13, 39.

    Google Scholar 

  • Kado, C., I. (2002). Crown gall. The Plant Health Instructor (online only). doi:10.1094/PHI-I-2002-1118-01

  • Lamichhane, J. R., Mazzaglia, A., Kshetri, M. B., Varvaro, L., & Balestra, G. M. (2009). First report of crown gall of Prunus spp. caused by Agrobacterium tumefaciens biovar 1 in Nepal. Journal of Plant Pathology, 91(S4), 104.

    Google Scholar 

  • Le Docte, A. (1927). Commercial determination of sugar in the beet root using the Sachs - Le Docte process. International Sugar Journal, 29, 488–492.

    CAS  Google Scholar 

  • Lindstrom, K., & Young, J. P. W. (2011). International Committee on Systematics of Prokaryotes Subcommittee on the taxonomy of Agrobacterium and Rhizobium: Minutes of the meeting. International Journal of Systematic and Evolutionary Microbiology, 61(12), 3089–3093. doi:10.1099/ijs.0.036913-0.

    Article  PubMed  Google Scholar 

  • Mahmoodi, B., Minassian, V., & Kashani, A. (1997). Occurrence of leaf and crown wart disease, caused by Urophlyctis leproides its importance and effect on sugar beet yield and quality in Khuzestan, Iran. Iranian Journal of Plant Pathology, 33, 22–25.

    Google Scholar 

  • Moore, L. W., Bouzar, H., & Burr, T. J. (2001). Gram-negative bacteria: Agrobacterium. In N. W. Schaad, J. B. Jones, & W. Chun (Eds.), Laboratory guide for identification of plant pathogenic bacteria (Third ed.). St. Paul: APS 379pp.

    Google Scholar 

  • Mougel, C., Thioulouse, J., Perriere, G., & Nesme, X. (2002). A mathematical method for determining genome divergence and species delineation using AFLP. International Journal of Systematic and Evolutionary Microbiology, 52, 573–586. doi:10.1099/00207713-52-2-573.

    Article  CAS  PubMed  Google Scholar 

  • Nagy, R., Rikeb, A. J., & Peterson, W. H. (1938). Some physiological studies of crown gall and contiguous tissue. Journal of Agricultural Research, 57, 545–555.

    CAS  Google Scholar 

  • Nyvall, R., F. (1979). Field crop diseases handbook. The Avi publishing company, Inc., Westport. 436pp.

  • Portier, P., Fischer-Le Saux, M., Mougel, C., Lerondelle, C., Chapulliot, D., Thioulouse, J., & Nesme, X. (2006). Identification of Genomic Species in Agrobacterium Biovar 1 by AFLP Genomic Markers. Applied and Environmental Microbiology, 72(11), 7123–7131. doi:10.1128/aem.00018-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puławska, J., & Kałużna, M. (2011). Phylogenetic relationship and genetic diversity of Agrobacterium spp. isolated in Poland based on gyrB gene sequence analysis and RAPD. European Journal of Plant Pathology, 133, 379–390. doi:10.1007/s10658-011-9911-2.

    Article  Google Scholar 

  • Rouhrazi, K., & Rahimian, H. (2012). Genetic diversity of Iranian Agrobacterium strains from grapevine. Annals of Microbiology, 62, 1661–1667. doi:10.1007/s13213-012-0423-x.

    Article  Google Scholar 

  • Shahabi, M. A. M., Taghavi, S. M., & Djavaheri, M. (2012). Phenotypic and genotypic characteristics of Agrobacterium isolates from different hosts in Fars and Kohgiluye and Boyerahmad provinces. Iranian Journal of Plant Pathology, 48(3), 113–115.

    Google Scholar 

  • Soltaninezhad, S., Mahmoudi, S. B., & Farokhi, N. R. (2008). Characterization of sugar beet Rhizoctonia isolates in Iran. Journal of Sugar Beet, 23, 135–150.

    Google Scholar 

  • Taghavi, S. M., & Golkhandan, E. (2006). Distribution and etiology of crown gall of sugar beet in Fars and Kohgiluye & Boyreahmad provinces. Iranian Journal of Plant Pathology, 42(3), 439–457.

    Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729. doi:10.1093/molbev/mst197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Townsend, C. O. (1915). Field studies of the crown gall of sugar beets. Bulletin of the U.S. Department of Agriculture. No: 203.

  • Westphal, A. (2013). Vertical distribution of Heterodera schachtii under susceptible, resistant, or tolerant sugar beet cultivars. Plant Disease, 97(1), 101–106. doi:10.1094/PDIS-05-12-0476-RE.

    Article  Google Scholar 

  • Yamamoto, S., & Harayama, S. (1995). PCR amplification and direct sequencing of gyrB genes with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Applied and Environmental Microbiology, 61(3), 1104–1109.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young, J. M., Kuykendall, L. D., Martı’nez-Romero, E., Kerr, A., & Sawada, H. (2001). A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. International Journal of Systematic and Evolutionary Microbiology, 51, 89–103.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Protection, College of Agriculture, Shiraz University, Shiraz, 71441-65186, Iran

    Hamzeh Mafakheri, S. Mohsen Taghavi, Zia Banihashemi & Ebrahim Osdaghi

  2. Eco-Innov Research Unit, INRA, Thiverval-Grignon, France

    Jay Ram Lamichhane

Authors
  1. Hamzeh Mafakheri
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  2. S. Mohsen Taghavi
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  3. Zia Banihashemi
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  4. Ebrahim Osdaghi
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  5. Jay Ram Lamichhane
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Correspondence to Ebrahim Osdaghi.

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Mafakheri, H., Taghavi, S.M., Banihashemi, Z. et al. Pathogenicity, host range and phylogenetic position of Agrobacterium species associated with sugar beet crown gall outbreaks in Southern Iran. Eur J Plant Pathol 147, 721–730 (2017). https://doi.org/10.1007/s10658-016-1034-3

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