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Microbial Ecology and Diversity
Diversity of Bacteriophages Infecting Xanthomonas oryzae pv. oryzae in Paddy Fields and Its Potential to Control Bacterial Leaf Blight of Rice
1Division of Biotechnology, Chonbuk National University, Iksan, 570-752, Republic of Korea, 2Advanced Institute of Environment and Bioscience, and Plant Medical Research Center, Chonbuk National University, Iksan, 570-752, Republic of Korea
Received: February 10, 2014; Accepted: March 14, 2014
J. Microbiol. Biotechnol. 2014; 24(6): 740-747
Published June 28, 2014 https://doi.org/10.4014/jmb.1402.02013
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
Bacterial leaf blight (BLB) caused by Xanthomonas oryzae pv. oryzae (Xoo) is a very serious
disease in rice-growing regions of the world. In spite of their economic importance, there are
no effective ways of protecting rice plants from this disease. Bacteriophages infecting Xoo
affect the population dynamics of the pathogen and consequently the occurrence of the
disease. In this study, we investigated the diversity, host range, and infectivity of Xoo phages,
and their use as a bicontrol agent on BLB was tested. Among the 34 phages that were isolated
from floodwater in paddy fields, 29 belonged to the Myoviridae family, which suggests that the
dominant phage in the ecosystem was Myoviridae. The isolated phages were classified into two
groups based on plaque size produced on the lawn of Xoo. In general, there was a negative
relationship between plaque size and host range, and interestingly the phages having a
narrow host range had low efficiency of infectivity. The deduced protein sequence analysis of
htf genes indicated that the gene was not a determinant of host specificity. Although the
difference in host range and infectivity depending on morphotype needs to be addressed, the
results revealed deeper understanding of the interaction between the phages and Xoo strains
in floodwater and damp soil environments. The phage mixtures reduced the occurrence of
BLB when they were treated with skim milk. The results indicate that the Xoo phages could be
used as an alternative control method to increase the control efficacy and reduce the use of
agrochemicals.
Keywords
Bacteriophage, Diversity, Bacterial leaf blight, Xanthomonas oryzae
References
- Ackermann HW. 1996. Frequency of morphological phage descriptions in 1995. Arch. Virol. 141: 209-218.
- Ackermann HW. 1999. Tailed bacteriophages. The order Caudovirales. Adv. Virus Res. 51: 135-201.
- Ackermann HW. 2001. Frequency of morphological phage descriptions in the year 2000. Arch. Virol. 146: 843-857.
- Bigby D, Kropinski AMB. 1989. Isolation and characterization of a Pseudomonas aeruginosa bacteriophage with a very limited host range. Can. J. Microbiol. 35: 630-635.
- Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, et al. 2002. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. USA 99:14250-14255.
- Brussow H, Hendrix RW. 2002. Phage genomics: small is beautiful. Cell 108: 13-16.
- Civerolo EL, Keil HL. 1969. Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59: 1966-1967.
- Deveau H, Van Calsteren MR, Moineaul S. 2002. Effect of exopolysaccharides on phage–host interactions in Lactococcus lactis. Appl. Environ. Microbiol. 68: 4364-4369.
- Flaherty JE, Harbaugh BK, Jones JB, Somodi GC. 2001. Hmutant bacteriophages as a potential biocontrol of bacterial blight of Geranium. HortScience 36: 98-100.
- Gill JJ, Svircev AM, Smith R, Castle AJ. 2003. Bacteriophages of Erwinia amylovora. Appl. Environ. Microbiol. 69: 2133-2138.
- Goodridge LD. 2004. Bacteriophage biocontrol of plant pathogens: fact or fiction? Trends Biotechnol. 22: 384-385.
- Inoue Y, Matsuura T, Ohara T, Azegami K. 2006. Sequence analysis of the genome of OP2, a lytic bacteriophage of Xanthomonas oryzae pv. oryzae. J. Gen. Plant Pathol. 172: 104110.
- Inoue Y, Matsuura T, Ohara T, Azegami K. 2006. Bacteriophage OP1, lytic for Xanthomonas oryzae pv. oryzae, changes its host range by duplication and deletion of the small domain in the deduced tail fiber gene. J. Gen. Plant Pathol. 172: 111-118.
- Jackson LE. 1989. Bacteriophage prevention and control of harmful plant bacteria. US Patent No. 4,828,999.
- Jones JB, Jackson LE, Balogh B, Obradovic A, Iriarte FB, Momol MT. 2007. Bacteriophages for plant disease control. Annu. Rev. Phytopathol. 45: 245-262.
- Kimura M, Jia ZJ, Nakayama N, Asakawa S. 2008. Ecology of viruses in soils: past, present and future perspectives. Soil Sci. Plant Nutr. 54: 1-32.
- Kuo T-T, Cheng L-C, Yang C-M, Yang S-E. 1971. Bacterial leaf blight of rice plant IV. Effect of bacteriophage on the infectivity of Xanthomonas oryzae. Bot. Bull. Acad. Sinica 12:1-9.
- Kuo T-T, Huang T-C, Wu R-Y, Chen C-P. 1968. Phage Xp12 of Xanthomonas oryzae (Uyeda et Ishiyama) Dowson. Can. J. Microbiol. 14: 1139-1142.
- Kuo T-T, Huang T-C, Chow T-Y. 1969. A filamentous bacteriophage from Xanthomonas oryzae. Virology 39: 548-555.
- Kuo T-T, Huang T-C, Wu R-Y, Yang C-M. 1967. Characterization of three bacteriophages of Xanthomonas oryzae (Uyeda et Ishiyama) Dowson. Bot. Bull. Acad. Sinica 8: 246-254.
- Lee C-N, Hu R-M, Chow T-Y, Lin J-W, Cheb H-Y, Tseng YH, Weng S-F. 2007. Comparison of genomes of three Xanthomonas oryzae bacteriophages. BMC Genomics 8: 442453.
- Lin N, You BY, Huang CY, Kuo CW, Wen FS, Yang JS, Tseng YH. 1994. Characterization of two novel filamentous phages of Xanthomonas. J. Gen. Virol. 75: 2543-2547.
- Maniloff J, Ackermann HW. 1998. Taxonomy of bacterial viruses, establishment of tailed virus genera and the other Caudovirales. Arch. Virol. 143: 2051-2063.
- Obradovic A, Jones JB, Momol MT, Olson SM, Jackson LE, Balogh B, et al. 2005. Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis. 89: 712-716.
- Okabe N, Goto M. 1963. Bacteriophages of plant pathogens. Annu. Rev. Phytopathol. 1: 397-418.
- Park S C, S himamura I, Fukunaga M , Mori K I, N akai T . 2000. Isolation of bacteriophages specific to a fish pathogen, Pseudomonas plecoglossicida, as a candidate for disease control. Appl. Environ. Microbiol. 66: 1416-1422.
- Shin MS, Noh TH, Kim KK, Shin SH, Ko KJ, Lee JK. 2005. Reaction of Korean rice varieties to new bacterial blight race, K3a. Korean J. Crop Sci. 50: 151-155.
- Sinha RP. 1980. Alteration of host specificity to lytic bacteriophages in Streptococcus cremoris. Appl. Environ. Microbiol. 40: 326-332.
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 27312739.
- Thomas RC. 1935. A bacteriophage in relation to Stewart’s disease of corn. Phytopathology 25: 371-372.
- Vidaver AK. 1976. Prospects for control of phytopathogenic bacteria by bacteriophages and bacteriocins. Annu. Rev. Phytopathol. 14: 451-465.
- Wakimoto SS. 1960. Classification of strains of Xanthomonas oryzae on the basis of their susceptibility against bacteriophages. Ann. Phytopathol. Soc. Jpn. 25: 193-198.
- Wolf A, Wiese J, Jost G, Witzel KP. 2003. Wide distribution of bacteriophages that lyse the same indigenous freshwater isolate (Sphingomonas sp. strain B18). Appl. Environ. Microbiol. 69: 2395-2398.
- Yuzenkova J, Nechaev S, Berlin J, Rogulja D, Kuznedelov K, Inman R, et al. 2003. Genome of Xanthomonas oryzae bacteriophage Xp10: an odd T-odd phage. J. Mol. Biol. 330:735-748.
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Research article
J. Microbiol. Biotechnol. 2014; 24(6): 740-747
Published online June 28, 2014 https://doi.org/10.4014/jmb.1402.02013
Copyright © The Korean Society for Microbiology and Biotechnology.
Diversity of Bacteriophages Infecting Xanthomonas oryzae pv. oryzae in Paddy Fields and Its Potential to Control Bacterial Leaf Blight of Rice
Jong-Chan Chae 1, 2, Nguyen Bao Hung 1, Sang-Mi Yu 1, Ha Kyung Lee 1 and Yong Hoon Lee 1, 2*
1Division of Biotechnology, Chonbuk National University, Iksan, 570-752, Republic of Korea, 2Advanced Institute of Environment and Bioscience, and Plant Medical Research Center, Chonbuk National University, Iksan, 570-752, Republic of Korea
Received: February 10, 2014; Accepted: March 14, 2014
Abstract
Bacterial leaf blight (BLB) caused by Xanthomonas oryzae pv. oryzae (Xoo) is a very serious
disease in rice-growing regions of the world. In spite of their economic importance, there are
no effective ways of protecting rice plants from this disease. Bacteriophages infecting Xoo
affect the population dynamics of the pathogen and consequently the occurrence of the
disease. In this study, we investigated the diversity, host range, and infectivity of Xoo phages,
and their use as a bicontrol agent on BLB was tested. Among the 34 phages that were isolated
from floodwater in paddy fields, 29 belonged to the Myoviridae family, which suggests that the
dominant phage in the ecosystem was Myoviridae. The isolated phages were classified into two
groups based on plaque size produced on the lawn of Xoo. In general, there was a negative
relationship between plaque size and host range, and interestingly the phages having a
narrow host range had low efficiency of infectivity. The deduced protein sequence analysis of
htf genes indicated that the gene was not a determinant of host specificity. Although the
difference in host range and infectivity depending on morphotype needs to be addressed, the
results revealed deeper understanding of the interaction between the phages and Xoo strains
in floodwater and damp soil environments. The phage mixtures reduced the occurrence of
BLB when they were treated with skim milk. The results indicate that the Xoo phages could be
used as an alternative control method to increase the control efficacy and reduce the use of
agrochemicals.
Keywords: Bacteriophage, Diversity, Bacterial leaf blight, Xanthomonas oryzae
References
- Ackermann HW. 1996. Frequency of morphological phage descriptions in 1995. Arch. Virol. 141: 209-218.
- Ackermann HW. 1999. Tailed bacteriophages. The order Caudovirales. Adv. Virus Res. 51: 135-201.
- Ackermann HW. 2001. Frequency of morphological phage descriptions in the year 2000. Arch. Virol. 146: 843-857.
- Bigby D, Kropinski AMB. 1989. Isolation and characterization of a Pseudomonas aeruginosa bacteriophage with a very limited host range. Can. J. Microbiol. 35: 630-635.
- Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, et al. 2002. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. USA 99:14250-14255.
- Brussow H, Hendrix RW. 2002. Phage genomics: small is beautiful. Cell 108: 13-16.
- Civerolo EL, Keil HL. 1969. Inhibition of bacterial spot of peach foliage by Xanthomonas pruni bacteriophage. Phytopathology 59: 1966-1967.
- Deveau H, Van Calsteren MR, Moineaul S. 2002. Effect of exopolysaccharides on phage–host interactions in Lactococcus lactis. Appl. Environ. Microbiol. 68: 4364-4369.
- Flaherty JE, Harbaugh BK, Jones JB, Somodi GC. 2001. Hmutant bacteriophages as a potential biocontrol of bacterial blight of Geranium. HortScience 36: 98-100.
- Gill JJ, Svircev AM, Smith R, Castle AJ. 2003. Bacteriophages of Erwinia amylovora. Appl. Environ. Microbiol. 69: 2133-2138.
- Goodridge LD. 2004. Bacteriophage biocontrol of plant pathogens: fact or fiction? Trends Biotechnol. 22: 384-385.
- Inoue Y, Matsuura T, Ohara T, Azegami K. 2006. Sequence analysis of the genome of OP2, a lytic bacteriophage of Xanthomonas oryzae pv. oryzae. J. Gen. Plant Pathol. 172: 104110.
- Inoue Y, Matsuura T, Ohara T, Azegami K. 2006. Bacteriophage OP1, lytic for Xanthomonas oryzae pv. oryzae, changes its host range by duplication and deletion of the small domain in the deduced tail fiber gene. J. Gen. Plant Pathol. 172: 111-118.
- Jackson LE. 1989. Bacteriophage prevention and control of harmful plant bacteria. US Patent No. 4,828,999.
- Jones JB, Jackson LE, Balogh B, Obradovic A, Iriarte FB, Momol MT. 2007. Bacteriophages for plant disease control. Annu. Rev. Phytopathol. 45: 245-262.
- Kimura M, Jia ZJ, Nakayama N, Asakawa S. 2008. Ecology of viruses in soils: past, present and future perspectives. Soil Sci. Plant Nutr. 54: 1-32.
- Kuo T-T, Cheng L-C, Yang C-M, Yang S-E. 1971. Bacterial leaf blight of rice plant IV. Effect of bacteriophage on the infectivity of Xanthomonas oryzae. Bot. Bull. Acad. Sinica 12:1-9.
- Kuo T-T, Huang T-C, Wu R-Y, Chen C-P. 1968. Phage Xp12 of Xanthomonas oryzae (Uyeda et Ishiyama) Dowson. Can. J. Microbiol. 14: 1139-1142.
- Kuo T-T, Huang T-C, Chow T-Y. 1969. A filamentous bacteriophage from Xanthomonas oryzae. Virology 39: 548-555.
- Kuo T-T, Huang T-C, Wu R-Y, Yang C-M. 1967. Characterization of three bacteriophages of Xanthomonas oryzae (Uyeda et Ishiyama) Dowson. Bot. Bull. Acad. Sinica 8: 246-254.
- Lee C-N, Hu R-M, Chow T-Y, Lin J-W, Cheb H-Y, Tseng YH, Weng S-F. 2007. Comparison of genomes of three Xanthomonas oryzae bacteriophages. BMC Genomics 8: 442453.
- Lin N, You BY, Huang CY, Kuo CW, Wen FS, Yang JS, Tseng YH. 1994. Characterization of two novel filamentous phages of Xanthomonas. J. Gen. Virol. 75: 2543-2547.
- Maniloff J, Ackermann HW. 1998. Taxonomy of bacterial viruses, establishment of tailed virus genera and the other Caudovirales. Arch. Virol. 143: 2051-2063.
- Obradovic A, Jones JB, Momol MT, Olson SM, Jackson LE, Balogh B, et al. 2005. Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis. 89: 712-716.
- Okabe N, Goto M. 1963. Bacteriophages of plant pathogens. Annu. Rev. Phytopathol. 1: 397-418.
- Park S C, S himamura I, Fukunaga M , Mori K I, N akai T . 2000. Isolation of bacteriophages specific to a fish pathogen, Pseudomonas plecoglossicida, as a candidate for disease control. Appl. Environ. Microbiol. 66: 1416-1422.
- Shin MS, Noh TH, Kim KK, Shin SH, Ko KJ, Lee JK. 2005. Reaction of Korean rice varieties to new bacterial blight race, K3a. Korean J. Crop Sci. 50: 151-155.
- Sinha RP. 1980. Alteration of host specificity to lytic bacteriophages in Streptococcus cremoris. Appl. Environ. Microbiol. 40: 326-332.
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 27312739.
- Thomas RC. 1935. A bacteriophage in relation to Stewart’s disease of corn. Phytopathology 25: 371-372.
- Vidaver AK. 1976. Prospects for control of phytopathogenic bacteria by bacteriophages and bacteriocins. Annu. Rev. Phytopathol. 14: 451-465.
- Wakimoto SS. 1960. Classification of strains of Xanthomonas oryzae on the basis of their susceptibility against bacteriophages. Ann. Phytopathol. Soc. Jpn. 25: 193-198.
- Wolf A, Wiese J, Jost G, Witzel KP. 2003. Wide distribution of bacteriophages that lyse the same indigenous freshwater isolate (Sphingomonas sp. strain B18). Appl. Environ. Microbiol. 69: 2395-2398.
- Yuzenkova J, Nechaev S, Berlin J, Rogulja D, Kuznedelov K, Inman R, et al. 2003. Genome of Xanthomonas oryzae bacteriophage Xp10: an odd T-odd phage. J. Mol. Biol. 330:735-748.
