A novel subspecies-specific primer targeting the gyrase B gene for the detection of Pectobacterium carotovorum subsp. brasiliense
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Abstract. Joko T, Soffan A, Muhammad Saifur Rohman MS. 2019. A novel subspecies-specific primer targeting the gyrase B gene for the detection of Pectobacterium carotovorum subsp. brasiliense. Biodiversitas 20: 3042-3048. Pectobacterium carotovorum subsp. brasiliense is one of the major causative bacterial pathogens of the soft rot disease in various crops. It has a high virulence and a wide range of hosts in the tropics and the subtropics. Most often, conventional methods are not able to accurately distinguish P. carotovorum subsp. brasiliense from other subspecies. Thus, this study aimed to design a specific gyrase B gene (gyrB) -based primers for the detection and identification of soft rot pathogen. The specific primers design was based on the alignment using gyrB gene sequence data from P. carotovorum subsp. brasiliense and other data from the GenBank. The primers comprised of F-gyr-Pcb (5’-CAC AGG CAC CGC TGG CTG TT-3’) and R-gyr-Pcb (5’-CGT CGT TCC ACT GCA ATG CCA-3’) with an amplicon of 336 base pairs. The specificity of the primers pair was verified both in silico and in polymerase chain reaction (PCR) assays, where the primers could only detect P. carotovorum subsp. brasiliense. Primers’ sensitivity was determined by qualitative PCR with a detection limit of less than 0.5 ng/µL of genomic DNA. Hence, the proposed detection tool can be beneficial to advance further studies on the ecology and epidemiology of soft rot diseases.
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References
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Charkowski A, Blanco C, Condemine G, Expert D, Franza T, Hayes C, Hugouvieux-Cotte-Pattat N, Solanilla EL, Low D, Moleleki L, Pirhonen M, Pitman A, Perna N, Reverchon S, Palenzuela PR, San Francisco M, Toth I, Tsuyumu S, van der Waals J, van der Wolf J, Van Gijsegem F, Yang CH, Yedidia I. 2012. The role of secretion systems and small molecules in soft-rot enterobacteriaceae pathogenicity. Annual Review of Phytopathology 50: 425?429.
Chuan LY, Cheng YH, Yang CH. 2013. Specific primer design for the polymerase chain reaction. Biotechnology Letter 35: 1541–1549.
Dauga C. 2002. Evolution of the gyrB gene and the molecular phylogeny of enterobacteriaceae: a model molecule for molecular systematic studies. International Journal of Systematic and Evolutionary Microbiology 52: 531–547.
Dees MW, Lysøe E, Rossmann S, Perminow J, Brurberg MP. 2017. Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology 67: 5222–5229.
Dieffenbach CW, Lowe TM, Dveksler GS. 1993. General concepts for PCR primer design. Genome Research 3: S30–S37.
Duarte V, De Boer SH, Ward LJ, De Oliveira AMR. 2004. Characterization of atypical Erwinia carotovora strains causing blackleg of potato in Brazil. Journal of Applied Microbiology 96: 535–545.
Dwimartina F, Arwiyanto T, Joko T. 2017. Potential of endophytic and rhizobacteria as an effective biocontrol for Ralstonia syzygii subsp. syzygii. Asian Journal of Plant Pathology 11: 191–198.
Frank JA, Reich CL, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. 2008. Critical evaluation of two primers commonly use for amplification of bacterial 16S rRNA Genes. Applied and Enviromental Microbiology 74: 2461–2470.
Gottsberger RA, Huss H. 2016. Pectobacterium carotovorum subsp. brasiliensis causing a soft rot on Styrian oil pumpkin in Austria. New Disease Reports 33: 12.
Hall TA. 1999. Bioedit: A user friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acid Symposium Series 41: 95–98.
Ismiyatuningsih, Joko T, Hartono S. 2016. Survey and detection of Pectobacterium atrosepticum in major potato-growing areas in Central Java province, Indonesia. Ilmu Pertanian 1: 1?6.
Joko T, Subandiyah S and Somowiyarjo S. 2000. The role of extracellular protein on the pathogenicity of Xanthomonas campestris pv. citri. Jurnal Perlindungan Tanaman Indonesia 6: 32?38.
Joko T, Hirata H, Tsuyumu S. 2007a. Sugar transporter (MfsX) of major facilitator superfamily is required for flagella-mediated pathogenesis in Dickeya dadantii 3937. Journal of General Plant Pathology 73: 266?273.
Joko T, Hirata H, Tsuyumu S. 2007b. A sugar transporter (MfsX) is also required by Dickeya dadantii 3937 for in planta fitness. Journal of General Plant Patholology 73: 274?280.
Joko T, Koentjoro MP, Somowiyarjo S, Rohman MS, Liana A, Ogawa N. 2012. Response of rhizobacterial communities in watermelon to infection with cucumber green mottle mosaic virus as revealed by cultivation-dependent RISA. Archives of Phytopathology and Plant Protection 45: 1810?1818.
Joko T, Subandi A, Kusumandari N, Wibowo A, Priyatmojo A. 2014. Activities of plant cell wall-degrading enzymes by bacterial soft rot of orchid. Archives of Phytopathology and Plant Protection 47: 1239?1250.
Joko T, Umehara M, Murata T, Etoh H, Izumori K, Tsuyumu S. 2018. Hyperinduction of pectate lyase in dickeya chrysanthemi EC16 by plant-derived sugars. Journal of Plant Interaction 13: 141?150.
Kasai H, Watanabe K, Gasteiger E, Bairoch A, Isono K, Yamamoto S, Harayama S. 1998. Construction of the gyrB database for the identification and classification of bacteria. Proceeding of International Conference on Genomic Informatics. P. 13?21.
Khayi S, Cigna J, Chong TM, Quetu-Laurent A, Chan K, Helias V, Faure D. 2016. Transfer of the potato plant isolates of Pectobacterium wasabiae to Pectobacterium parmentieri sp. nov. International Journal of Systematic and Evolutionary Microbiology 66: 5379?5383.
Lee CS, Wetzel K, Buckley T, Wozniak D, Lee J. 2011. Rapid and sensitive detection of Pseudomonas aeruginosa in chlorinated water and aerosols targeting gyrB gene using real-time PCR. Journal of Applied Microbiology 111: 893?903.
Lee DH, Kim JB, Lim JA, Han SW, Heu S. 2014. Genetic diversity of Pectobacterium carotovorum subsp. brasiliensis isolated in Korea. Plant Pathology Journal 30: 117?124.
Ma B, Hibbing ME, Kim HS, Reedy RM, Yedidia I, Breuer J, Glasner JD, Perna NT, Kelman A, Charkowski AO. 2007. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97: 1150?1163.
Maeda Y, Shinohara H, Kiba A, Ohnishi K, Furuya N, Kawamura Y, Ezaki T, Vandamme P, Tsushima S, Hikichi Y. 2006. Phylogenetic study and multiplex PCR-based detection of Burkholderia plantarii, Burkholderia glumae and Burkholderia gladioli using gyrB and rpoD sequences. International Journal of Systematic and Evolutionary Microbiology 56: 1031–1038.
Mahfut, Joko T, Daryono BS. 2016. Molecular characterization of odontoglossum ring spot virus (ORSV) in Java and Bali, Indonesia. Asian Journal of Plant Pathology 10: 9?14.
Nabhan S, Boer SH, Maiss E, Wydra K. 2012a. Taxonomic relatedness between Pectobacterium carotovorum subsp. carotovorum, Pectobacterium carotovorum subsp. odoriferum and Pectobacterium carotovorum subsp. brasiliense subsp. nov. Journal of Applied Microbiology 113: 904?13.
Nabhan S, Wydra K, Linde M, Debener T. 2012b. The use of two complementary DNA assays, AFLP and MLSA, for epidemic and phylogenetic studies of pectolytic enterobacterial strains with focus on the heterogeneous species Pectobacterium carotovorum. Plant pathology 61: 498?508.
Nabhan S, De Boer SH, Maiss E, Wydra K. 2013. Pectobacterium aroidearum sp. nov., a soft rot pathogen with preference for monocotyledonous plants. International Journal of Systematic and Evolutionary Microbiology 63: 2520–2525.
Nurjanah N, Joko T, Subandiyah S. 2017. Characterization of Pantoea ananatis isolated from garlic and shallot. Jurnal Perlindungan Tanaman Indonesia 21: 120?126.
Oulghazi S, Cigna J, Lau YY, Moumni M, Chan KG, Faure D. 2019. Transfer of the waterfall source isolate Pectobacterium carotovorum M022 to Pectobacterium fontis sp. nov., a deep-branching species within the genus Pectobacterium. International Journal of Systematic and Evolutionary Microbiology 69: 470?475.
Perombelon MCM, Kelman A. 1980. Ecology of the soft rot erwinias. Annual Review of Phytopathology 18: 361?387.
Pei YA, Oberdorf WE, Nossa CW, Agarwal A, Chokshi P, Gerz AA, Jin Z, Lee P, Yang L, Poles M, Brown SM, Sotero S, De Santis T, Brodie E, Nelson K, Pei Z. 2010. Diversity of 16S rRNA genes with individual prokaryotic genomes. Applied and Environmental Microbiology 76: 3886–3897.
Pédron J, Bertrand C, Taghouti G, Portier P, Barny MA. 2019. Pectobacterium aquaticum sp. nov., isolated from waterways. International Journal of Systematic and Evolutionary Microbiology 69: 745-751.
Poretsky R, Rodriguez RLM, Luo C, Tsementzi D, Konstantinidis KT. 2014. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE 9: e93827.
Sarfraz S, Riaz K, Oulghazi S, Cigna J, Sahi ST, Khan SH, Faure D. 2018. Pectobacterium punjabense sp. nov., isolated from blackleg symptoms of potato plants in Pakistan. International Journal of Systematic and Evolutionary Microbiology 68: 3551–3556.
Seo ST, Furuya N, Lim CK, Takanami Y, Tsuchiya K. 2002. Phenotypic and genomic diversity of Erwinia carotovora subsp. carotovora strains from Asia. Journal of Phytopathology 150: 120?127.
Shirshikov FV, Korzhenkov AA, Miroshnikov KK, Kabanova AP, Barannik AP, Ignatov AN, Miroshnikov KA. 2018. Draft genome sequences of new genomospecies “Candidatus Pectobacterium maceratum” strains, which cause soft rot in plants. Genome Announcement 6: e00260?18.
Sutrisno, Susanto F A, Wijayanti P, Retnoningrum M D, Nuringtyas T R, Joko T, Purwestri Y A. 2018. Screening of resistant Indonesian black rice cultivars against bacterial leaf blight. Euphytica 214: 199. https://doi.org/10.1007/s10681-018-2279-z.
Trianom B, Arwiyanto T, Joko T. 2018. Development of novel subspecies-specific primers based on the endoglucanase gene for detection of Ralstonia syzygii subsp. syzygii. Jurnal Perlindungan Tanaman Indonesia 22: 124?131.
Trianom B, Arwiyanto T, Joko T. 2019. Morphological and molecular characterization of Sumatra disease of clove in central java, Indonesia. Tropical Life Sciences Research 30: 107–118.
Van Pelt-Verkuit E, Van Belkum A, Hays JP. 2008. Principals and technical aspects of PCR amplification. Netherland: Springer. 30p.
Waleron M, Misztak A, Waleron M, Franczuk M, Wielgomas B, Waleron. 2018. Transfer of Pectobacterium carotovorum subsp. carotovorum strains isolated from potatoes grown at high altitudes to Pectobacterium peruviense sp. nov. Systematic and Applied Microbiology 41: 85–93.
Waleron M, Miztak A, Waleron M, Franczuk M, Jonca J, Wielgomas B, Mikici?ski A, Popovi? T, Waleron K. 2019a. Pectobacterium zantedeschiae sp. nov. a new species of a soft rot pathogen isolated from Calla lily (Zantedeschia spp.). Systematic and Applied Microbiology 42: 275–283.
Waleron M, Misztak A, Waleron M, Jonca J, Furmaniak M, Waleron K. 2019b. Pectobacterium polonicum sp. nov. isolated from vegetable fields International Journal of Systematic and Evolutionary Microbiology 69: 1751–1759.
Waleron M, Miztak A, Jonca J, Furmaniak M, Waleron MM, Waleron K. 2019c. First report of ‘Candidatus Pectobacterium maceratum’ causing soft rot of potato in Poland. Plant Disease, 103(6) (https://doi.org/10.1094/PDIS-11-18-2107-PDN).
Widyaningsih S, Utami SNH, Joko T, Subandiyah S. 2019. Plant response and huanglongbing disease development against heat treatments on ‘Siam Purworejo’ (Citrus nobilis (Lour)) and ‘Nambangan’ (C. maxima (Burm.) Merr.) under field condition. Archives of Phytopathology and Plant Protection 52: 259–276.
Windari U, Joko T, Subandiyah S. 2015. Detection of bacterial fruit blotch of melon using ELISA. Jurnal Perlindungan Tanaman Indonesia 19: 1–5.
Bhat KA, Masood SD, Bhat NA, Bhat MA, Razvi SM, Mir MR, Akhtar S, Wani N, Habib M. 2010. Current status of postharvest soft rot in vegetables: A review. Asian Journal of Plant Sciences 9: 200–208.
Charkowski A, Blanco C, Condemine G, Expert D, Franza T, Hayes C, Hugouvieux-Cotte-Pattat N, Solanilla EL, Low D, Moleleki L, Pirhonen M, Pitman A, Perna N, Reverchon S, Palenzuela PR, San Francisco M, Toth I, Tsuyumu S, van der Waals J, van der Wolf J, Van Gijsegem F, Yang CH, Yedidia I. 2012. The role of secretion systems and small molecules in soft-rot enterobacteriaceae pathogenicity. Annual Review of Phytopathology 50: 425?429.
Chuan LY, Cheng YH, Yang CH. 2013. Specific primer design for the polymerase chain reaction. Biotechnology Letter 35: 1541–1549.
Dauga C. 2002. Evolution of the gyrB gene and the molecular phylogeny of enterobacteriaceae: a model molecule for molecular systematic studies. International Journal of Systematic and Evolutionary Microbiology 52: 531–547.
Dees MW, Lysøe E, Rossmann S, Perminow J, Brurberg MP. 2017. Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology 67: 5222–5229.
Dieffenbach CW, Lowe TM, Dveksler GS. 1993. General concepts for PCR primer design. Genome Research 3: S30–S37.
Duarte V, De Boer SH, Ward LJ, De Oliveira AMR. 2004. Characterization of atypical Erwinia carotovora strains causing blackleg of potato in Brazil. Journal of Applied Microbiology 96: 535–545.
Dwimartina F, Arwiyanto T, Joko T. 2017. Potential of endophytic and rhizobacteria as an effective biocontrol for Ralstonia syzygii subsp. syzygii. Asian Journal of Plant Pathology 11: 191–198.
Frank JA, Reich CL, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. 2008. Critical evaluation of two primers commonly use for amplification of bacterial 16S rRNA Genes. Applied and Enviromental Microbiology 74: 2461–2470.
Gottsberger RA, Huss H. 2016. Pectobacterium carotovorum subsp. brasiliensis causing a soft rot on Styrian oil pumpkin in Austria. New Disease Reports 33: 12.
Hall TA. 1999. Bioedit: A user friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acid Symposium Series 41: 95–98.
Ismiyatuningsih, Joko T, Hartono S. 2016. Survey and detection of Pectobacterium atrosepticum in major potato-growing areas in Central Java province, Indonesia. Ilmu Pertanian 1: 1?6.
Joko T, Subandiyah S and Somowiyarjo S. 2000. The role of extracellular protein on the pathogenicity of Xanthomonas campestris pv. citri. Jurnal Perlindungan Tanaman Indonesia 6: 32?38.
Joko T, Hirata H, Tsuyumu S. 2007a. Sugar transporter (MfsX) of major facilitator superfamily is required for flagella-mediated pathogenesis in Dickeya dadantii 3937. Journal of General Plant Pathology 73: 266?273.
Joko T, Hirata H, Tsuyumu S. 2007b. A sugar transporter (MfsX) is also required by Dickeya dadantii 3937 for in planta fitness. Journal of General Plant Patholology 73: 274?280.
Joko T, Koentjoro MP, Somowiyarjo S, Rohman MS, Liana A, Ogawa N. 2012. Response of rhizobacterial communities in watermelon to infection with cucumber green mottle mosaic virus as revealed by cultivation-dependent RISA. Archives of Phytopathology and Plant Protection 45: 1810?1818.
Joko T, Subandi A, Kusumandari N, Wibowo A, Priyatmojo A. 2014. Activities of plant cell wall-degrading enzymes by bacterial soft rot of orchid. Archives of Phytopathology and Plant Protection 47: 1239?1250.
Joko T, Umehara M, Murata T, Etoh H, Izumori K, Tsuyumu S. 2018. Hyperinduction of pectate lyase in dickeya chrysanthemi EC16 by plant-derived sugars. Journal of Plant Interaction 13: 141?150.
Kasai H, Watanabe K, Gasteiger E, Bairoch A, Isono K, Yamamoto S, Harayama S. 1998. Construction of the gyrB database for the identification and classification of bacteria. Proceeding of International Conference on Genomic Informatics. P. 13?21.
Khayi S, Cigna J, Chong TM, Quetu-Laurent A, Chan K, Helias V, Faure D. 2016. Transfer of the potato plant isolates of Pectobacterium wasabiae to Pectobacterium parmentieri sp. nov. International Journal of Systematic and Evolutionary Microbiology 66: 5379?5383.
Lee CS, Wetzel K, Buckley T, Wozniak D, Lee J. 2011. Rapid and sensitive detection of Pseudomonas aeruginosa in chlorinated water and aerosols targeting gyrB gene using real-time PCR. Journal of Applied Microbiology 111: 893?903.
Lee DH, Kim JB, Lim JA, Han SW, Heu S. 2014. Genetic diversity of Pectobacterium carotovorum subsp. brasiliensis isolated in Korea. Plant Pathology Journal 30: 117?124.
Ma B, Hibbing ME, Kim HS, Reedy RM, Yedidia I, Breuer J, Glasner JD, Perna NT, Kelman A, Charkowski AO. 2007. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97: 1150?1163.
Maeda Y, Shinohara H, Kiba A, Ohnishi K, Furuya N, Kawamura Y, Ezaki T, Vandamme P, Tsushima S, Hikichi Y. 2006. Phylogenetic study and multiplex PCR-based detection of Burkholderia plantarii, Burkholderia glumae and Burkholderia gladioli using gyrB and rpoD sequences. International Journal of Systematic and Evolutionary Microbiology 56: 1031–1038.
Mahfut, Joko T, Daryono BS. 2016. Molecular characterization of odontoglossum ring spot virus (ORSV) in Java and Bali, Indonesia. Asian Journal of Plant Pathology 10: 9?14.
Nabhan S, Boer SH, Maiss E, Wydra K. 2012a. Taxonomic relatedness between Pectobacterium carotovorum subsp. carotovorum, Pectobacterium carotovorum subsp. odoriferum and Pectobacterium carotovorum subsp. brasiliense subsp. nov. Journal of Applied Microbiology 113: 904?13.
Nabhan S, Wydra K, Linde M, Debener T. 2012b. The use of two complementary DNA assays, AFLP and MLSA, for epidemic and phylogenetic studies of pectolytic enterobacterial strains with focus on the heterogeneous species Pectobacterium carotovorum. Plant pathology 61: 498?508.
Nabhan S, De Boer SH, Maiss E, Wydra K. 2013. Pectobacterium aroidearum sp. nov., a soft rot pathogen with preference for monocotyledonous plants. International Journal of Systematic and Evolutionary Microbiology 63: 2520–2525.
Nurjanah N, Joko T, Subandiyah S. 2017. Characterization of Pantoea ananatis isolated from garlic and shallot. Jurnal Perlindungan Tanaman Indonesia 21: 120?126.
Oulghazi S, Cigna J, Lau YY, Moumni M, Chan KG, Faure D. 2019. Transfer of the waterfall source isolate Pectobacterium carotovorum M022 to Pectobacterium fontis sp. nov., a deep-branching species within the genus Pectobacterium. International Journal of Systematic and Evolutionary Microbiology 69: 470?475.
Perombelon MCM, Kelman A. 1980. Ecology of the soft rot erwinias. Annual Review of Phytopathology 18: 361?387.
Pei YA, Oberdorf WE, Nossa CW, Agarwal A, Chokshi P, Gerz AA, Jin Z, Lee P, Yang L, Poles M, Brown SM, Sotero S, De Santis T, Brodie E, Nelson K, Pei Z. 2010. Diversity of 16S rRNA genes with individual prokaryotic genomes. Applied and Environmental Microbiology 76: 3886–3897.
Pédron J, Bertrand C, Taghouti G, Portier P, Barny MA. 2019. Pectobacterium aquaticum sp. nov., isolated from waterways. International Journal of Systematic and Evolutionary Microbiology 69: 745-751.
Poretsky R, Rodriguez RLM, Luo C, Tsementzi D, Konstantinidis KT. 2014. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS ONE 9: e93827.
Sarfraz S, Riaz K, Oulghazi S, Cigna J, Sahi ST, Khan SH, Faure D. 2018. Pectobacterium punjabense sp. nov., isolated from blackleg symptoms of potato plants in Pakistan. International Journal of Systematic and Evolutionary Microbiology 68: 3551–3556.
Seo ST, Furuya N, Lim CK, Takanami Y, Tsuchiya K. 2002. Phenotypic and genomic diversity of Erwinia carotovora subsp. carotovora strains from Asia. Journal of Phytopathology 150: 120?127.
Shirshikov FV, Korzhenkov AA, Miroshnikov KK, Kabanova AP, Barannik AP, Ignatov AN, Miroshnikov KA. 2018. Draft genome sequences of new genomospecies “Candidatus Pectobacterium maceratum” strains, which cause soft rot in plants. Genome Announcement 6: e00260?18.
Sutrisno, Susanto F A, Wijayanti P, Retnoningrum M D, Nuringtyas T R, Joko T, Purwestri Y A. 2018. Screening of resistant Indonesian black rice cultivars against bacterial leaf blight. Euphytica 214: 199. https://doi.org/10.1007/s10681-018-2279-z.
Trianom B, Arwiyanto T, Joko T. 2018. Development of novel subspecies-specific primers based on the endoglucanase gene for detection of Ralstonia syzygii subsp. syzygii. Jurnal Perlindungan Tanaman Indonesia 22: 124?131.
Trianom B, Arwiyanto T, Joko T. 2019. Morphological and molecular characterization of Sumatra disease of clove in central java, Indonesia. Tropical Life Sciences Research 30: 107–118.
Van Pelt-Verkuit E, Van Belkum A, Hays JP. 2008. Principals and technical aspects of PCR amplification. Netherland: Springer. 30p.
Waleron M, Misztak A, Waleron M, Franczuk M, Wielgomas B, Waleron. 2018. Transfer of Pectobacterium carotovorum subsp. carotovorum strains isolated from potatoes grown at high altitudes to Pectobacterium peruviense sp. nov. Systematic and Applied Microbiology 41: 85–93.
Waleron M, Miztak A, Waleron M, Franczuk M, Jonca J, Wielgomas B, Mikici?ski A, Popovi? T, Waleron K. 2019a. Pectobacterium zantedeschiae sp. nov. a new species of a soft rot pathogen isolated from Calla lily (Zantedeschia spp.). Systematic and Applied Microbiology 42: 275–283.
Waleron M, Misztak A, Waleron M, Jonca J, Furmaniak M, Waleron K. 2019b. Pectobacterium polonicum sp. nov. isolated from vegetable fields International Journal of Systematic and Evolutionary Microbiology 69: 1751–1759.
Waleron M, Miztak A, Jonca J, Furmaniak M, Waleron MM, Waleron K. 2019c. First report of ‘Candidatus Pectobacterium maceratum’ causing soft rot of potato in Poland. Plant Disease, 103(6) (https://doi.org/10.1094/PDIS-11-18-2107-PDN).
Widyaningsih S, Utami SNH, Joko T, Subandiyah S. 2019. Plant response and huanglongbing disease development against heat treatments on ‘Siam Purworejo’ (Citrus nobilis (Lour)) and ‘Nambangan’ (C. maxima (Burm.) Merr.) under field condition. Archives of Phytopathology and Plant Protection 52: 259–276.
Windari U, Joko T, Subandiyah S. 2015. Detection of bacterial fruit blotch of melon using ELISA. Jurnal Perlindungan Tanaman Indonesia 19: 1–5.
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