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Characteristic of Pseudomonas Syringae Pv. Atrofaciens Isolated from Weeds of Wheat Field

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Characteristic of Pseudomonas Syringae Pv. Atrofaciens Isolated from Weeds of Wheat Field applied sciences Article Characteristic of Pseudomonas syringae pv. atrofaciens Isolated from Weeds of Wheat Field Liudmyla Butsenko 1, Lidiia Pasichnyk 1 , Yuliia Kolomiiets 2, Antonina Kalinichenko 3,* , Dariusz Suszanowicz 3 , Monika Sporek 4 and Volodymyr Patyka 1 1 Zabolotny Institute of Microbiology and Virology, National Academy of Sciences of Ukraine, 03143 Kyiv, Ukraine; [email protected] (L.B.); [email protected] (L.P.); [email protected] (V.P.) 2 Department of Ecobiotechnology and Biodiversity, National University of Life and Environmental Sciences of Ukraine, 03143 Kyiv, Ukraine; [email protected] 3 Institute of Environmental Engineering and Biotechnology, University of Opole, 45-040 Opole, Poland; [email protected] 4 Institute of Biology, University of Opole, 45-040 Opole, Poland; [email protected] * Correspondence: [email protected]; Tel.: +48-787-321-587 Abstract: The aim of this study was the identification of the causative agent of the basal glume rot of wheat Pseudomonas syringae pv. atrofaciens from the affected weeds in wheat crops, and determination of its virulent properties. Isolation of P. syringae pv. atrofaciens from weeds of wheat crops was carried out by classical microbiological methods. To identify isolated bacteria, their morphological, cultural, biochemical, and serological properties as well as fatty acids and Random Amplification of Polymorphic DNA (RAPD)-PCR (Polymerase chain reaction) profiles with the OPA-13 primer were studied. Pathogenic properties were investigated by artificial inoculation of wheat plants and weed plants, from which bacteria were isolated. For the first time, bacteria that are virulent both for weeds and wheat were isolated from weeds growing in wheat crops. It was shown that the fatty acids profiles of the bacteria isolated from the weeds contained typical for P. syringae pv. Citation: Butsenko, L.; Pasichnyk, L.; atrofaciens fatty acids, in particular, hydroxy acids: 3-hydroxydecanoic, 2-hydroxydodecanoic, and Kolomiiets, Y.; Kalinichenko, A.; 3-hydroxydodecanoic. RAPD-PCR profiles of the newly isolated strains were identical to those of the Suszanowicz, D.; Sporek, M.; Patyka, P. syringae atrofaciens P. syringae atrofaciens V. Characteristic of Pseudomonas collection strains pv. UCM B-1011 and pv. UCM B-1014 syringae pv. atrofaciens Isolated from and contained a dominant fragment of 700 bp. The isolated strains, according to their phenotypic Weeds of Wheat Field. Appl. Sci. 2021, and genotypic properties, were identified as P. syringae pv. atrofaciens. It was established that the 11, 286. https://doi.org/10.3390/ causative agent of basal glume rot of wheat P. syringae pv. atrofaciens is polyphagous and capable of app11010286 infecting a wide range of plants. The main control measure for cereals diseases caused by P. syringae pv. Atrofaciens—crop rotations with nonhost species, should be revised, and alternative control Received: 3 November 2020 methods must be proposed. Accepted: 28 December 2020 Published: 30 December 2020 Keywords: Pseudomonas syringae pv. atrofaciens; basal glume rot; wheat; weeds; RAPD; fatty acids; phenotypic and genotypic properties Publisher’s Note: MDPI stays neu- tral with regard to jurisdictional clai- ms in published maps and institutio- nal affiliations. 1. Introduction Nowadays, around the world, researchers have noted the increasingly threatening spread and aggressiveness of phytopathogenic bacteria [1,2]. This trend is also observed in Copyright: © 2020 by the authors. Li- Ukraine [3,4]. This also applies to wheat, one of the most valuable and important grain censee MDPI, Basel, Switzerland. crops and ranks first in the world’s sown area [5]. Bacterial diseases spread data are This article is an open access article often not realistic, as they are based as a rule on observing symptoms without isolation of distributed under the terms and con- the pathogen and its identification [2]. Pseudomonas syringae pv. atrofaciens has been the ditions of the Creative Commons At- main causative agent of bacterial diseases of wheat, particularly basal glume rot of wheat, tribution (CC BY) license (https:// for many years [6–9]. The study of this pathogen’s biological properties, the patterns of creativecommons.org/licenses/by/ population formation and the circulation of pathogens, and techniques that will allow 4.0/). Appl. Sci. 2021, 11, 286. https://doi.org/10.3390/app11010286 https://www.mdpi.com/journal/applsci Appl. Sci. 2021, 11, 286 2 of 12 influencing these processes are of fundamental and practical importance and will not lose their relevance. The causative agent of the basal glume rot of wheat belongs to the species of Pseu- domonas syringae, which, according to much research, is the most important bacterial plant pathogen in terms of economics and scientific studies [10]. Pseudomonas syringae pv. atrofa- ciens causes basal glume rot of wheat in Russia, Bulgaria, Italy, Germany, New Zealand, and Iran [8,11]. The scientific literature data confirm the high harmfulness of this pathogen and its ability to cause epiphytotics [12]. This pathogen’s danger is its ability to colonize both the host plant and other plant species of the phyllosphere effectively. Forming epiphytic populations, which is the primary inoculum for plant infection, P. syringae pv. atrofaciens can cause mass plant damage when favorable weather conditions occur [13–15]. It is known that for a long time, the causative agent of the basal glume rot of wheat had been found as an epiphyte on non-crops plant species and also on annual and perennial weeds [14]. Weeds’ ability to serve as an ecological niche for agents of bacterial diseases that can affect crops has been discussed [16], and it was proved experimentally that weeds could serve as sources of dangerous epiphytic populations of phytopathogenic bacteria [17]. At the same time, the presence of the pathogens common both for cultivated plants and weeds in crops and the problem of the specialization of the pathogens that affect weeds remain unclear. Therefore, our study aimed to identify phytopathogenic bacteria on affected weeds in wheat crops and to establish their relationship with the causative agent of the basal glume rot of wheat. 2. Material and Methods Bacterial strains used in research. Strains of Pseudomonas syringae pv. atrofaciens, which are stored in the collection of microorganisms of the Department of phytopathogenic bacteria of the Zabolotny Institute of Microbiology and Virology of the National Academy of Sciences of Ukraine (NASU), Kyiv were used in the study: P. syringae pv. atrofaciens UCM B-1011 (PDDCC 4394), P. syringae pv. atrofaciens UCM B-1014, and P. syringae pv. atrofaciens 9780. Also, we used the type strain P. syringae pv. syringae UCM B-1027 (NCPPB 281). Isolation of P. syringae pv. atrofaciens. In order to detect the strains of P. syringae pv. atrofaciens, wheat fields in the Kyiv region, Ukraine (50◦05016.3” N 30◦02056.8” E) were surveyed 2019 and selected weed plants of Sonchus arvensis L. and Papaver argemone L. with symptoms of bacterial infection were collected. Bacteria isolation was carried out by plating the pieces of plants, pounded with 0.1 mL of sterile tap water, on potato agar. For the bacteria isolation, the parts of plants were selected on the border of healthy and damaged tissues. The morphology and structure of bacterial colonies were studied after 72 h growing on potato agar in Petri dishes [18]. Cell morphology and motility were determined in Gram-stained and “crushed drop” preparations, respectively, under a Sigeta MB-201 microscope using a one-day bacterial culture grown in nutrient broth (NB) [5,18]. For the initial selection of the isolates from weeds, the LOPAT test (Levan production, Oxidase, Protopectinase activity on potato, Arginine dihydrolase, hypersensitive reaction on Tobacco) was used [18]. Physiological and biochemical characterization. For studying the physiological and biochemical properties of the bacterial isolates from weeds, the test system NEFERMtest24 (MikroLaTEST®, ErbaLachema, Czech Republic) was used. Oxidase was detected in the cells of the isolated strains by test strips Bactident Oxidase (Merck, Germany). Fermentative and oxidative glucose metabolism (OF-test) were determined by the breakable microwell plate (OFtest, Erba Lachema). The ability to induce rot on potato was investigated by applying 0.01 mL of bacterial suspension (1 × 107 colony-forming unit (CFU)/mL) on potato discs [18]. Potato discs were incubated for 24 h at 25 ◦C, and then the presence of rot was registered. Pathogenicity tests. To study the virulent properties of isolated strains, artificial inoculation of S. arvensis and P. argemone plants, from which bacterial strains were obtained, Appl. Sci. 2021, 11, 286 3 of 12 was carried out under field conditions and of plants of the spring wheat variety Pecherianka in the greenhouse. Artificial infection of wheat seedlings seven days old was performed by pricking through a drop of bacterial suspension with a concentration of 1 × 107 CFU/mL. The development of visible symptoms of damage evidenced the bacterium virulence. The results of artificial infection were analyzed according to a 5-point scale in 10 days after the inoculation of bacteria [5]. Highly aggressive strains caused the damage from three to four scores, while weakly aggressive—1–2 scores. Aggressiveness was determined as the average score of disease symptoms in ten inoculated plants. Also, the pathogenic properties of bacteria that were isolated from
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