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Burkholderia Gladioli Associated with Soft Rot of Onion Bulbs in Poland

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Burkholderia Gladioli Associated with Soft Rot of Onion Bulbs in Poland Journal of Plant Pathology (2015), 97 (1), 37-43 Edizioni ETS Pisa, 2015 37 BURKHOLDERIA GLADIOLI ASSOCIATED WITH SOFT ROT OF ONION BULBS IN POLAND B. Kowalska, U. Smoli ´nska and M. Oskiera Research Institute of Horticulture. Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland SUMMARY (Gitaitis et al., 1998), Pantoea ananatis (Gitaitis et al., 2002; Walcott et al., 2002), Enterobacter cloacae (Schroeder et al., Bacterial diseases of onion (Allium cepa L.) are serious 2009), Burkholderia ambifaria and B. pyrrocinia (Jacobs et problems in Poland. In this study bacterial strains were al., 2008) and Serratia spp. (Beriam, 2007) have also been isolated from onion bulbs with soft-rot symptoms. Patho- reported as agents of onion bacterial diseases. genicity tests were conducted on onion bulbs and also on B. gladioli pv. alliicola was first reported as Phytomo- tobacco leaves on whose basis twelve isolates were chosen nas alliicola from rotten onion bulbs in New York state to further characterization. These isolates were identified (USA) (Starr and Burkholder, 1942); then, under the name using physiological and biochemical tests, and confirmed of Pseudomonas gladioli, from Iowa (USA), as the cause by species-specific PCR, ERIC-PCR and sequence analysis of yellowing and death of onion leaves and infection of of 16S rRNA, gyrB, lepA, phaC, recA gene fragments. All the outer scales of young bulbs (Semeniuk and Melthus, examined isolates were identified as Burkholderia gladioli. 1943). The bacterium was isolated from onion bulbs by It is the first report of the occurrence of B. gladioli on both Burkholder and Vitanov (Burkholder, 1950) who re- onion as the cause of onion disease in Poland. garded it exclusively as an onion bulb pathogen and was reclassified as Burkholderia gladioli (Yabuuchi et al., 1992). Key words: Burkholderia gladioli, onion, diagnosis, soft Its presence in onion has been reported from Europe, rot, disease. Asia and USA (Lee et al., 2005; Schwartz and Mohan, 2008; Stoyanova et al., 2011; Schroeder et al., 2012), with crop losses of up to 40%. INTRODUCTION B. gladioli strains have also been isolated from and re- garded as a pathogen of Gladiolus sp., Iris sp., Eustoma Onion (Allium cepa L.) is one of the major vegetable grandiflorum (Coenye and Vandamme, 2003; Stoyanova et crops grown in Poland, where the total area planted and al., 2007; Keith et al., 2005), summer snowflake (Leucojum harvested in 2012 was ca. 25,000 ha. Since onion harvest- aestivum) (Stoyanova et al., 2013), saffron (Crocus sativus L.) ing often coincides with rainy weather and during cultiva- (Fiori et al., 2011), maize (Lu et al., 2007; Gijon-Hernandez tion hailstorms may occur, complex bacterial and fungal et al., 2011) and rice (Ura et al., 2006; Nandakumar et al., diseases often develop. In recent years, bacterial diseases 2009). have caused very serious problems to Polish onion crops, B. gladioli can also be a human pathogen, but it can inflicting significant economic losses because they are dif- hardly be identified with commercial detection kits. Its ficult to control. Successful control depends on proper strains are sensitive to the complement-mediated lysis sanitation, avoiding injuries, keeping bulbs dry and cool of human serum, which confers a natural immunity to during storage, assuring good insect control and prac- healthy individuals. However, one of the four cases of hu- ticing crop rotation (Agrios, 2005). Bacterial soft rot of man infection was in a non-immunocompromised patient onion bulbs is most frequent and it can appear during (Stoyanova et al., 2007). cultivation, storage or transportation (Sobiczewski and Very little is known on B. gladioli occurrence in Poland Schollenberger, 2002). and the characteristics of its strains. There are only a few Soft-rot diseases of bacterial origin, particularly those short reports on onion soft rot induced by Burkholderia sp. associated with Burkholderia gladioli, B. cepacia, Pectobac- (Sobiczewski and Schollenberger, 2002), but no informa- terium carotovorum subsp. carotovorum (Schwartz and tion on the biochemical and molecular properties of the Mohan, 2008; Yohalem and Lorbeer, 1997), Serratia plymu- associated bacteria, except for a paper by Schollenberger thica (Kowalska et al., 2011) are known all over the word. and Zamorski (2008) who observed atypical disease symp- Pseudomonas marginalis (Kim et al., 2002; El-Hendawy, toms on lisianthus growing in greenhouses near Warsaw. 2004), Pseudomonas syringae, Pseudomonas viridiflava The bacterium isolated from diseased plants was identi- fied as B. gladioli by conventional microbiological meth- Corresponding author: B. Kowalska Fax: +48.46.8333186 ods, and the disease was named bacterial ring blight of E-mail: [email protected] lisianthus (Schollenberger and Zamorski, 2008). 38 Burkholderia gladioli in Poland Journal of Plant Pathology (2015), 97 (1), 37-43 Table 1. Bacterial strains used in this study and GeneBank accession Nos. GenBank accession No. Bacterial isolates Locality, place and year of isolation gltB lepA phaC recA Bg259 Poland, Tomaszów Lubelski; field; 2006 - KF857500 KF857513 KF857525 Bg260 Poland, Tomaszów Lubelski; field; 2006 KF857489 KF857501 - KF857526 Bg261 Poland, Tomaszów Lubelski; field; 2006 KF857490 KF857502 KF857514 KF857527 Bg285 Poland, Radom; field; 2006 KF857491 KF857503 KF857515 - Bg294 Poland, Radom; field; 2006 KF857492 KF857504 KF857516 KF857528 Bg295 Poland, Radom; field; 2006 KF857493 KF857505 KF857517 KF857529 Bg435 Poland, Skierniewice; storage; 2007 KF857494 KF857506 KF857518 KF857530 Bg469 Poland, Skierniewice; storage; 2007 - KF857507 KF857519 KF857531 Bg467 Poland, Skierniewice; storage; 2007 KF857495 KF857508 KF857520 KF857532 Bg494 Poland, Skierniewice; field; 2008 KF857496 KF857509 KF857521 KF857533 Bg500 Poland, Skierniewice; field; 2008 KF857497 KF857510 KF857522 KF857534 Bg514 Poland, Hopkie; storage; 2008 KF857498 KF857511 KF857523 KF857535 B. gladioli pv. alliicola LMG 6979 USA KF857488 KF857499 KF857512 KF857524 B. cepacia LMG 6962 USA - - - - The objective of this study was the identification of each piece was wounded with a laboratory needle to make bacteria associated with soft rot of onion in Poland, using a wound 3-4 mm in diameter which was inoculated with biochemical and molecular methods. 20 µl suspension from a 24 h pure bacterial culture con- taining 1.0-2.5 × 108 CFU ml−1. Controls were not inoculat- ed. Inoculations of reference strains B. cepacia LMG 6962 MATERIALS AND METHODS and B. gladioli LMG 6979 were also made consisting of two replicates (six onion pieces) for each bacterial strain. Isolation of soft rotting bacteria. Onion bulbs with Disease symptoms were examined after 4 days incubation bacterial soft rot were obtained during summer and au- at 28°C. Virulence was evaluated using an arbitrary scale tumn of 2006, 2007 and 2008 from Polish onion storage from 0 (no tissue maceration) to 3 (complete maceration). warehouses or field crops. The bulbs were washed with tap The experiment was repeated twice. For the experiments water and cut lengthwise. Diseased scale tissues were then that followed only the isolates were used that induced mac- cut into about 10-15 mm cubes with a sterilized scalpel, the eration of level two and greater than two. A total of 12 fragments were sterilized in ethanol for 30 sec, washed in isolates were investigated: Bg259, Bg260, Bg261, Bg285, sterile water and plated onto nutrient agar medium (NA, Bg294, Bg295, Bg435, Bg467, Bg469, Bg494, Bg500 and beef extract 3 g, glucose 2.5 g, peptone 5 g, agar 15 g, and Bg514 (Table 1). distilled water 1000 ml). Petri dishes with NA were incu- Tobacco hypersensitivity reaction was conducted us- bated at 28°C for 48 h. Next, a selected bacterial colony ing tobacco plants of cv. Samsun (Klement et al., 1964). A was streaked onto a fresh NA plate and used for this study. bacterial suspension of 1.0-2.5 × 108 CFU ml−1 was injected into the intercellular space of tobacco leaves, recording as Bacterial strains and culture conditions. Forty two positive the complete collapse of the tissues after 24 h. The bacterial isolates used in this study were maintained at test was repeated with each isolate at least twice. −80ºC in nutrient broth medium containing 50% (v/v) glycerol. The isolates were transferred onto NA, incubat- Biochemical and physiological tests. For these assays ed at 28°C for 24 h and maintained at 4°C for short-term 12 bacterial isolates were used, that gave positive responses use. Genuine isolates of B. gladioli pv. alliicola LMG 6979 in pathogenicity tests. Bacterial colony morphology was and B. cepacia LMG 6962, provided by from a Belgian assessed on NA medium taking into account the shape, Microorganism Collection (Ghent University) were used size, texture and markings of the surface. Physiological for comparison. and biochemical characterization was according to Schaad et al. (2001). The following properties were determined: Pathogenicity tests. All strains were examined for Gram reaction by 3% KOH (Suslow et al., 1982) and the ability to macerate onion tissue. To this aim, healthy Gram stain, anaerobic growth in Hugh and Leifson (1953) bulbs of cv. Grabowska were peeled, washed with run- medium, production of fluorescent pigment on King B ning water and sterilized in 70% ethanol for 30 sec and medium [peptone 20.0 g, K2HPO4 2.5 g, glycerol 15 ml, in 0.5% NaOCl for 5 min. The bulbs were then washed MgSO4 × 7H2O 6.0 g, agar 15.0 g, water 1000 ml (King et in sterile water and cut lengthwise into two parts. Three al., 1954)]; colony colour on YDC medium [yeast extract onion pieces were placed into a large Petri dish incuba- 10.0 g, glucose 20.0 g, CaCO3 20.0 g, agar 15.0 g, water tion chamber (volume 314 cm3), on a paper filter which had 1000 ml (Wilson et al., 1967)]; growth on D1M medium been wetted with 10 ml of sterile water. The outer scale of [cellobiose 5.0 g, NH4Cl 1.0 g, NaH2PO4 1.0 g, K2HPO4 Journal of Plant Pathology (2015), 97 (1), 37-43 Kowalska et al.
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