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Xanthomonads and Other Yellow-Pigmented Xanthomonas-Like Bacteria Associated with Tomato Seeds in Tanzania

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Xanthomonads and Other Yellow-Pigmented Xanthomonas-Like Bacteria Associated with Tomato Seeds in Tanzania African Journal of Biotechnology Vol. 11(78), pp. 14303-14312, 27 September, 2012 Available online at http://www.academicjournals.org/AJB DOI:10.5897/AJB12.1305 ISSN 1684-5315 ©2012 Academic Journals Full Length Research Paper Xanthomonads and other yellow-pigmented Xanthomonas-like bacteria associated with tomato seeds in Tanzania E. R. Mbega1,2*, E. G. Wulff1, R. B. Mabagala2, J. Adriko1,3, O. S. Lund1 and C. N. Mortensen1 1Danish Seed Health Centre for Developing Countries, Department of Plant and Environmental Sciences, University of Copenhagen, Denmark. 2African Seed Health Centre, Department of Crop Science and Production, Sokoine University of Agriculture, Tanzania. 3National Agricultural Research Laboratories, Kawanda, Uganda. Accepted 3 August, 2012 Tomato (Solanum lycopersicum L.) seeds habour unique bacterial community that can be pathogenic or beneficial to their host. Xanthomonas causing bacterial leaf spot (BLSX) on tomato and other yellow- pigmented xanthomonads-like bacteria (XLB) that closely resemble BLSX were obtained from tomato seeds collected from Northern, Central and Southern highland regions of Tanzania. A total of 73 strains were isolated from 52 seed samples of 15 tomato cultivars. Results obtained with Biolog and sequence analysis of the 16S rRNA gene showed that samples originating from Central Tanzania harbored the most diverse populations of XLB and BLSX as compared to Northern and Southern Tanzania. The predominant bacterial genera in tomato seeds were Stenotrophomonas, Sphingomonas, Chryseobacterium, Xanthomonas, Pantoea and Flavobacterium. All strains identified by Biolog as Xanthomonas with exception of Xanthomonas campestris pv. malvacearum, were pathogenic on tomato and pepper plants. Strains identified by Biolog as Sphingomonas sanguinis and Sphingomonas terrae also incited black rot symptoms on pepper leaves. However, bacterial strains belonging to the genus Stenotrophomonas, Chryseobacterium, Pantoea and Flavobacterium were not pathogenic on tomato and pepper. Phylogenetic analysis showed that strains of the genus Xanthomonas are more closely related to Stenotrophomonas and Pantoea compared to the other bacterial genera found in tomato seeds. Key words: Xanthomonas, yellow-pigmented bacteria, seed, tomato, phylogeny. INTRODUCTION Members of the genus Xanthomonas are Gram-negative, vesicatoria (Xv), Xanthomonas perforans (Xp) and aerobic, yellow pigment-producing bacteria that belong to Xanthomonas gardneri (Xg), are associated with BLS of the class of γ-proteobacteria, many of which are plant tomato (Jones et al., 2004, 2006). In addition to these pathogens (Hayward, 1993). Bacterial leaf spot (BLS) species, Xanthomonas campestris pv. raphani and caused by Xanthomonas spp. is one of the most serious Xanthomonas arboricola have been reported as BLS seed-borne diseases of tomato (Solanum lycopersicum pathogens of tomato (Westcott and Horst, 2001; Punina L.) in Tanzania (Black et al., 2001; Kaaya et al., 2003, et al., 2009) and hot pepper plants, respectively (Myung Shenge, 2007). Four species of the genus Xanthomonas, et al., 2010). namely Xanthomonas euvesicatoria (Xeu), Xanthomonas Infested tomato seed is often reported as the primary source of the pathogen (McGuire and Jones, 1989). Therefore, a number of methods for detection of BLS pathogens in tomato seeds have been developed, *Corresponding author. E-mail: [email protected]. including liquid assays with semi-selective media Tel: +255 754 649 585. Fax: +255 232 600 574 (McGuire et al., 1986, McGuire and Jones, 1989; 14304 Afr. J. Biotechnol. Table 1. Tomato seed samples collected from three growing zones in Tanzania used in the current study. Origin of seed sample Variety/cultivar DSHC accession number Northern Central Southern zone zone highland zone Cal-J 48638, 48667, 48668, 48674, 48678 + + + 48639, 48647, 48649, 48651, 48656, 48662, 48664, 48667, Tanya + + + 48669, 8728, 48729, 48730, 48834, 48836, 48837, 48838, 48862 Money maker 48644, 48653 + + + Romeco 48646 - - + Tengeru 97 28654, 48659, 48671 + + + Vikima DK* 48676 - + - Onyx 48670, 48672, 48679 - + - Mpwipwi-local 48658 - - + Mshumaa 48648, 48657, 48660, + + + RomaVFN 48655, 48673, 48680 + + + Kituruma-local 48642 + - - Israel 48652 - - + Dumdum-local 48640, 48641,48645, 48650, 48663, 48666, 48675, 48681, 48835 + + + Rio Grande 48677 - + - VF 311 48643 - + - DSHC=Danish Seed Health Centre; -=absent; +=commonly found; * named by farmers as ‘Vikima DK’ (name of the supplier company). Sijam et al., 1992), along with biochemical tests and or evaluating the pathogenicity of the different bacterial the Biolog identification system (Jones et al., 1993; strains on tomato and sweet pepper, and 3) examining Shenge et al., 2007), nucleic acid analysis (Leite et al., their genetic relationship based on phylogenetic analysis 1995; Kuflu and Cuppels, 1997; Obradodivic et al., 2004; of 16S rRNA gene sequences. Mbega et al., 2010) and pathogenicity tests (Lelliot and Stead, 1987; ISF, 2007). Seed-associated Xanthomonas- like bacteria (XLB) that closely resemble the BLS-causing MATERIALS AND METHODS xanthomonads (BLSX) are also commonly found in tomato seeds, but currently very limited information on Seed samples these bacterial communities is available (Gitaitis et al., Farmer-saved seeds of tomato were collected from three main 1987). These microorganisms grow fast on agar media tomato-growing zones in Tanzania namely the Northern, Central and appear to interfere with the isolation and ability of and Southern highland zones, in July 2008. A total of 52 tomato recovery of the BLSX from tomato seeds (ISF, 2007). At seed samples of 15 different commonly-grown cultivars were present, most of the existing data on bacterial microflora randomly collected from 45 different locations (Table 1). The survey of tomato seed is restricted to seed-borne pathogens covered one farm in Kilimanjaro, five in Iringa, seven in Tanga, seven in Mbeya, nine in Rukwa and sixteen farms in Morogoro (Black et al., 2001; Kaaya et al., 2003; Shenge et al., regions. 2007) and does not include information on example other bacterial species, their distribution and genetic relation- ships. Tomatoes grown from locally-produced seeds Isolation of bacteria from seed have been reported to harbour unique populations of xanthomonads (Gitaitis et al., 1987; Punina et al., 2009). The hand halving method was used to obtain working seed Knowledge on these microbial populations can be useful samples for seed health assays using a standardized procedure described by International Seed Testing Association (ISTA, 2005). to improve the isolation of pathogenic bacteria from For isolation of bacteria, sub-samples of 1000 to 10000 seeds were tomato seed in seed health assays and to reveal their incubated in phosphate buffer saline (PBS)-Tween buffer (0.05 M of pathogenic or pro-biotic potential in tomato and related PO4, pH 7.2; 8.5 g of NaCl; 20 ml of Tween 20; 1000 ml of distilled hosts. water) for 14 to 20 h at 4 to 10°C (ISF, 2007). Aliquots of 100 µL This study aimed at 1) assessing genus and/ or species from the undiluted, 1:10 and 1:100 dilutions in duplicate were plated onto: (1) mTMB medium (10 g of bacto peptone, 0.1 g of H BO , 10 composition of yellow-pigmented, Xanthomonads and 3 3 g of KBr, 0.25 g of CaCl2 anhydrous, 15 g of bacto agar, 10 ml of Xanthomonas-like bacteria associated with tomato seed Tween 80, 65 mg of cephalexin, 12 mg of 5-fluorouracil, 0.2 g of in three different tomato-growing zones in Tanzania; 2) tobramycin sulphate, 100 mg of cycloheximide and 1000 ml of Mbega et al. 14305 distilled water) (McGuire et al., 1986) and (2) CKTM medium (Sijam sweet pepper (Capsicum annuum L.) cultivars that are known to be et al., 1992) (2 g of soya peptone, 2 g of tryptone, 1 g of glucose, 1 susceptible to BLSX. Therefore, seed lots of the tomato cultivar g of L-glutamine, 6 g of L-histidine, 0.8 g of (NH4)2 HPO4, 1 g of Tanya and Moneymaker and the sweet pepper cultivar Early KH2PO4, 0.4 g of MgSO4.7H2O, 0.25 g of CaCl2 anhydrous, 15 g of Calwonder, found to be free of BLS pathogen(s) by liquid assays Bacto agar, 10 ml of Tween 80, 65 mg of cephalexin, 12 mg of 5- (ISF, 2007), were used in the pathogenicity tests. Prior to sowing, fluorouracil, 0.4 g of tobramycin sulphate, 100 mg of bacitracin, 10 the seeds were surface-disinfected in 70% ethanol for 1 min, g of neomycin sulphate, 100 mg of cycloheximide and 1000 ml of followed by immersion in 1% of sodium hypochlorite for 3 min, distilled water). rinsed three times consecutively in sterile distilled water and left to Inoculated plates were incubated at 28°C for 3 to 7 days and dry under the flow cabinet for 1 to 2 h. Seeds were then sown in were observed for the presence of yellow-pigmented colonies daily. pots of 8 cm diameter containing peat soil (Pindstrup substrate Reference strains of BLSX were used as positive controls and No.2, Pindstrup Mosebrug A/S, Denmark) and sand (3:1), included strains obtained from the National Collection of Plant respectively and kept in growth chamber at 25 to 30°C under high Pathogenic Bacteria (NCPPB), UK. namely, X. euvesicatoria relative humidity (> 85%). The abaxial surfaces of four 14-day-old (NCPPB 2968), X. vesicatoria (NCPPB 422), X. vesicatoria tomato and 21-day-old sweet pepper seedlings per strain were (NCPPB 476), X. perforans (NCPPB 4321), X. gardneri (NCPPB spray-inoculated to runoff with an inoculum suspension of 108 881) and strains isolated from tomato (XVT 12 and XVT 28) and CFU/ml (OD600 = 0.01) prepared from 24 h-old bacterial cultures pepper (XVP 129 and XVP 196) received as X. campestris pv. grown on NA at 28°C. The inoculated seedlings were subsequently vesicatoria (courtesy of Dr Jaw-Fen Wang from the World covered with polyethylene bags and kept in the growth chamber for Vegetable Centre in Taiwan). Two yellow-pigmented bacterial 14 days. Seedlings sprayed with sterile saline water (containing pathogens of tomato served as negative controls in the evaluations, 0.85% of NaCl) alone were used as a negative control and namely strain NCPPB 2445 (Pseudomonas corrugata) and IPO 542 seedlings sprayed with suspensions prepared from the BLSX (Clavibacter michiganensis subsp.
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