Abstract
During July 2015 to June 2017, 63 walnut and 94 stone fruit orchards were surveyed in Iran to identify and characterize the causal agent of a disease inducing leaf spot and fruit canker symptoms. Altogether, 189 Prunus spp. and 141 walnut samples (i.e. leaves, branches and fruits) were collected from 10 Provinces in northern, northwestern, central and southern Iran. Forty-three yellow-pigmented Gram-negative bacterial isolates were recovered from symptomatic plants. Only seven bacterial strains isolated from walnut in Mazandaran and Golestan Provinces were identified as X. arboricola pv. juglandis based on pathogenicity assays, specific PCRs, and multilocus sequence analysis. Based on the phenotypic features and phylogenetic analysis of gyrB gene sequences, strains isolated from stone fruit trees were identified as multiple Pantoea species (i.e. P. agglomerans, P. ananatis, P. vagans and P. pleuroti). None of these strains caused symptoms on Prunus spp. plantlets tested under greenhouse conditions. Although the occurrence of bacterial blight of walnut in Iran was ascertained using molecular-phylogenetic analysis, no evidence was obtained that the observed disease was the same as the bacterial spot and canker of stone fruits caused by X. arboricola pv. pruni in the country.
References
Adriko J, Mbega ER, Mortensen CN, Wulff EG, Tushemereirwe WK, Kubiriba J, Lund OS (2014) Improved PCR for identification of members of the genus Xanthomonas. Eur J Plant Pathol 138:293–306
Ahmadi S, Harighi B, Abdollahzadeh J (2018) Phylogenetic relationships of fluorescent pseudomonad isolates associated with bacterial canker of stone fruit trees in Kurdistan Province, Iran. Eur J Plant Pathol 150:679–689
Amani B (1977) Bacterial blight of walnut in Iran. Iranian J Plant Pathol 13:14–23
Anonymous (2014) Agricultural statistics. Vol. 1. 2012–13 cropping seasons. Ministry of Jihad-e-Agriculture, Tehran
Banihashemi Z (1990) Biology and control of Polystigma oehraceum, the cause of almond red leaf blotch. Plant Pathol 39:309–315
Barnett HL, Hunter BB (1998) Illustrated Genera of Imperfect Fungi, 4th edn. APS Press, St. Paul
Borhani B, Rahimian H (2015) Cryptococcus adeliensis inciting branch canker on stone fruit trees. Eur J Plant Pathol 145:71–80
Boudon S, Manceau C, Nottéghem JL (2005) Structure and origin of Xanthomonas arboricola pv. pruni populations causing bacterial spot of stone fruit trees in Western Europe. Phytopathology 95:1081–1088
EPPO (2006) OEPP/EPPO, Bulletin OEPP/EPPO Bulletin 36: 129–133
Falahi Charkhabi N, Shams-bakhsh M, Rahimian H (2010) Genetic diversity among Brreneria nigrifluens strains in Iran. Eur J Plant Pathol 128:303–310
FAOSTAT (2015) Food and Agriculture Organization of the United Nations, FAOSTAT database, available at http://faostat.fao.org/. Accessed Dec 2017
Fargier E, Fischer-Le Saux M, Manceau C (2011) A multilocus sequence analysis of Xanthomonas campestris reveals a complex structure within crucifer-attacking pathovars of this species. Syst Appl Microbiol 34:156–165
Giovanardi D, Dallai D, Stefani E (2016) Population features of Xanthomonas arboricola pv. pruni from Prunus spp. orchards in northern Italy. Eur J Plant Pathol 147:761–771
Habibi H, Khodaygan P (2015) The first report of Stenotrophomonas sp. associated with canker and leaf spot disease of stone fruits in Iran. Iranian J Plant Pathol 51:103–106
Jami F, Kazempour M, Elahinia S, Khodakaramian G (2005) First report of Xanthomonas arboricola pv. pruni on stone fruit trees from Iran. J Phytopathol 153:371–372
Jones AL (1995) Cherry leaf spot. In: Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K, Uyemoto JK (eds) Compendium of stone fruit diseases. APS Press, St. Paul, MN, USA, pp 21–22
Lalancette N, McFarland KA (2007) Phytotoxicity of copper-based bactericides to peach and nectarine. Plant Dis 91:1122–1130
Lamichhane JR, Fabi A, Varvaro L (2014) Bacterial species associated to brown spots of hazelnut in Central Italy: survey, isolation and characterization. In VIII International Congress on Hazelnut 1052:243–251
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. Bioinformatics 23:2947–2948
Lee YA, Sung AN, Liu TF, Lee YS (2009) Combination of chromogenic differential medium and estA-specific PCR for isolation and detection of phytopathogenic Xanthomonas spp. Appl Environ Microbiol 75:6831–6838
Mafakheri H, Taghavi SM, Banihashemi Z, Osdaghi E, Lamichhane JR (2017) 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
Merda D, Bonneau S, Guimbaud JF, Durand K, Brin C, Boureau T, Lemaire C, Jacques MA, Fischer-Le Saux M (2016) Recombination-prone bacterial strains form a reservoir from which epidemic clones emerge in agrosystems. Environ Microbiol Rep 8:572–581
Moragrega C, Matias J, Aletà N, Montesinos E, Rovira M (2011) Apical necrosis and premature drop of Persian (English) walnut fruit caused by Xanthomonas arboricola pv. juglandis. Plant Dis 95:1565–1570
Osdaghi E (2014) Occurrence of common bacterial blight on mungbean (Vigna radiata) in Iran caused by Xanthomonas axonopodis pv. phaseoli. New Dis Rep 30:9
Osdaghi E, Rahimi Kakavandi N (2015) A new leaf disease on Populus euphratica in South-Western Iran. For Pathol 45:336–341
Osdaghi E, Shams-Bakhsh M, Alizadeh A, Lak MR (2010) Study on common bean seed lots for contamination with Xanthomonas axonopodis pv. phaseoli by BIO-PCR technique. Int J Agri Tech 6:503–513
Osdaghi E, Taghavi SM, Fazliarab A, Elahifard E, Lamichhane JR (2015a) Characterization, geographic distribution and host range of Curtobacterium flaccumfaciens: an emerging bacterial pathogen in Iran. Crop Prot 78:185–192
Osdaghi E, Pakdaman Sardrood B, Bavi M, Akbari Oghaz N, Kimiaei S, Hadian S (2015b) First report of Curtobacterium flaccumfaciens pv. flaccumfaciens causing cowpea bacterial wilt in Iran. J Phytopathol 163:653–656
Osdaghi E, Taghavi SM, Hamzehzarghani H, Lamichhane JR (2016a) Occurrence and characterization of the bacterial spot pathogen Xanthomonas euvesicatoria on pepper in Iran. J Phytopathol 64:722–734
Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM, Lamichhane JR (2016b) Occurrence and characterization of a new red-pigmented variant of Curtobacterium flaccumfaciens, the causal agent of bacterial wilt of edible dry beans in Iran. Eur J Plant Pathol 146:129–145
Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Lamichhane JR (2017) Monitoring the occurrence of tomato bacterial spot and range of the causal agent Xanthomonas perforans in Iran. Plant Pathol 66:990–1002
Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM, Tegli S, Lamichhane JR (2018a) Epiphytic Curtobacterium flaccumfaciens strains isolated from symptomless solanaceous vegetables are pathogenic on leguminous but not on solanaceous plants. Plant Pathol 67:388–398
Osdaghi E, Ansari M, Taghavi SM, Zarei S, Koebnik R, Lamichhane JR (2018b) Pathogenicity and phylogenetic analysis of Clavibacter michiganensis strains associated with tomato plants in Iran. Plant Pathol 67:957–970
Palacio-Bielsa A, Pothier JF, Roselló M, Duffy B, López MM (2012) Detection and identification methods and new tests as developed and used in the framework of cost 873 for bacteria pathogenic to stone fruits and nuts. J Plant Pathol 94:135–146
Pothier JF, Pagani MC, Pelludat C, Ritchie DF, Duffy B (2011) A duplex-PCR method for species-and pathovar-level identification and detection of the quarantine plant pathogen Xanthomonas arboricola pv. pruni. J Microbiolo Methods 86:16–24
Saremi H, Amiri ME (2010) Evaluation of resistance to anthracnose (Marssonina juglandis) among diverse Iranian clones of walnut (Juglans regia L.). J Food Agric Environ 8:375–378
Schaad NW, Jones JB, Chun W (2001) Laboratory Guide for Identification of Plant Pathogenic Bacteria, 3rd edn. APS Press, St. Paul
Sedighian N, Shams-Bakhsh M, Osdaghi E, Khodaygan P (2014) Etiology and host range of bacterial leaf blight and necrosis of squash and muskmelon in Iran. J Plant Pathol 96:507–514
Sedighian N, Taghavi SM, Osdaghi E, Shams-Bakhsh M (2018) Serratia marcescens associated with squash leaf chlorosis and necrotic spots in Iran. J Plant Pathol 100:85–89
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Temperini CV, Pardo AG, Pose GN (2017) First report of apical necrosis in walnut cultivars from northern Argentinean Patagonia. J Plant Pathol Microbiol 8(7). https://doi.org/10.4172/2157-7471.1000414
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols. A Guide to Methods and Applications. Ed. by Innis MA, Gelfand DH, Sninsky JJ, San Diego USA: Academic Press, pp. 315–322
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. Appl Environ Microbiol 61:1104–1109
Yaripour Z, Taghavi SM, Osdaghi E, Lamichhane JR (2018) Host range and phylogenetic analysis of Xanthomonas alfalfae causing bacterial leaf spot of alfalfa in Iran. Eur J Plant Pathol 150:267–274
Young JM, Park DC, Shearman HM, Fargier E (2008) A multilocus sequence analysis of the genus Xanthomonas. Syst Appl Microbiol 31:366–377
Zarei S, Taghavi SM, Hamzehzarghani H, Osdaghi E, Lamichhane JR (2018) Epiphytic growth of Xanthomonas arboricola and Xanthomonas citri on non-host plants. Plant Pathol 67:660–670
Funding
This research was funded by Shiraz University, Shiraz, Iran.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The result of this work has not been published previously and is not under consideration elsewhere.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Fig. S1
Agarose gel electrophoresis of PCR products using the Xanthomonas- (a - b) and X. arboricola-specific (c) primers in this study. Primers X-ITS-F3j, X-ITS-F3k, X-ITS-F3c, X-ITS F3d/X-ITS-R2 (a) directed the amplification of the expected 254 bp DNA fragment in all the bacterial strain isolated from stone fruits and walnut trees. Whereas, primer pair Xc-lip-F2/Xc-lip-R2 (b) directed the amplification of the expected 777 bp DNA fragment only in the Xanthomonas arboricola strains isolated from walnut trees. X. arboricola-specific primer pair XarbQ-F/XarbQ-R directed the amplification of the expected 402 bp DNA fragment in all the X. arboricola strains isolated from walnut, however, either unspecific amplification or wrong sized fragment amplification were observed in the Pantoea spp. strains isolated from stone fruits (c). Lanes: M: 100 bp DNA Ladder, 1–5: X. arboricola strains isolated from walnut trees in Iran, 6–19: Pantoea spp. strains isolated from stone fruits, and 20: DNA-free control. (JPG 791 kb)
Rights and permissions
About this article
Cite this article
Zarei, S., Taghavi, S.M., Banihashemi, Z. et al. Etiology of leaf spot and fruit canker symptoms on stone fruits and nut trees in Iran. J Plant Pathol 101, 1133–1142 (2019). https://doi.org/10.1007/s42161-019-00283-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42161-019-00283-w