Research Article
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Determination of the host range of Pectobacterium polaris causing bacterial soft rot disease

Year 2022, , 234 - 240, 01.08.2022
https://doi.org/10.37908/mkutbd.1064147

Abstract

Aims: Pectobacterium polaris is a novel species of Pectobacterium taxa, which was reported in different regions of the world and has been recently detected in Turkey. In this study, in order to determine the host range of this novel species, two representative strains were evaluated in terms of their pathogenicity on several host plants, and it is aimed to determine plant species under the risk of the pathogen.

Methods and Results: P. polaris strains NV3 and NV19, isolated from potato plants showing blackleg symptoms in Nevşehir province during the vegetation period of 2019, were used for artificial inoculation. Bacterial suspension of both strains was inoculated by injecting into the red cabbage, broccoli, cauliflower, onion, garlic, carrot, tomato, pepper, eggplant, cucumber, squash, melon, watermelon, lettuce, sunflower and sugar beet plants. The appearance of the disease symptoms indicated that both strains of P. polaris caused disease in all the plant species inoculated artificially. Viable bacterial colonies were re-isolated from infected plant tissue.

Conclusions: Pectobacterium species are very destructive bacterial plant pathogens that cause soft rot on numerous plant species. It has been determined that P. polaris, which has been reported in different regions of the world and in Turkey as a new emerging pathogen within in a wide host range. Disease protection precautions should be taken in the regions where the pathogen is isolated for the first time, and especially pathogen transmission should be prevented to the clean production areas by potato tubers.

Significance and Impact of the Study: All tested plant species were determined as potential hosts for P. polaris. The risk status of the pathogen on these plants, which have economic importance in Turkey, was determined for the first time with this study

Supporting Institution

Yozgat Bozok University

Project Number

6602c-ZF/21-472

Thanks

This study was supported by financial grant of project management office, Yozgat Bozok University, project no 6602c-ZF/21-472. The author would like to sincerely thank Prof. Dr. Soner SOYLU for valuable comments and important criticisms, and Ahmet DEMİRCİ for diligent proofreading on the manuscript

References

  • Agrios GN (2006) Bacterial soft rots, 5th edn. Academic Press, San Diego.
  • Aytop Y, Çukadar, M, Şahin A (2014) Agricultural sector profile of Turkey in the world. Türk Tarım ve Doğa Bilimleri Dergisi, 1(Özel Sayı-1), 688-694.
  • Cariddi C, Bubici G (2016) First report of bacterial pith soft rot caused by Pectobacterium carotovorum subsp. brasiliense on artichoke in Italy. Journal of Plant Pathology, 563-568.
  • Caruso A, Licciardello G, La Rosa R, Catara V, Bella P (2016) Mixed infection of Pectobacterium carotovorum subsp. carotovorum and P. carotovorum subsp. brasiliensis in tomato stem rot in Italy. Journal of Plant Pathology, 98(3), 661-665.
  • Charkowski AO (2007) The soft rot Erwinia. In Plant-associated bacteria (pp. 423-505). Springer, Dordrecht.
  • Chen C, Li X, Bo Z, Du W, Fu L, Tian, Y, Cui S, Shi Y, Xie H (2021) Occurrence, Characteristics, and PCR-Based Detection of Pectobacterium polaris Causing Soft Rot of Chinese Cabbage in China. Plant Disease, 105(10), 2880-2887.
  • Czajkowski R, Perombelon MC, van Veen JA, van der Wolf JM (2011) Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: a review. Plant pathology, 60(6), 999-1013.
  • Czajkowski R, Pérombelon MCM, Jafra S, Lojkowska E, Potrykus M, Van Der Wolf, JM, Sledz W (2015) Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: a review. Annals of Applied Biology 166(1): 18-38.
  • Dadaşoğlu F, Kotan R (2017) Identification and characterization of Pectobacterium carotovorum. J Anim Plant Sci, 27, 647-654.
  • De Boer SH, Li X, Ward LJ (2012) Pectobacterium spp. associated with bacterial stem rot syndrome of potato in Canada. Phytopathology 102(10): 937-947.
  • Dees MW, Lysøe E, Rossmann S, Perminow J, Brurberg MB (2017) Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology, 67(12), 5222-5229.
  • 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(3): 535-545.
  • Gardan L, Gouy C, Christen R, Samson R (2003) Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. International journal of systematic and evolutionary microbiology, 53(2), 381-391.
  • Khayi S, Cigna J, Chong TM, Quêtu-Laurent A, Chan KG, Hélias 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(12), 5379-5383.
  • Hélias V, Hamon P, Huchet E, Wolf JVD, Andrivon D (2012) Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya. Plant Pathology 61(2): 339-345.
  • Lee DH, Kim JB, Lim JA, Han SW, Heu S (2014) Genetic diversity of Pectobacterium carotovorum subsp. brasiliensis isolated in Korea. The plant pathology journal, 30(2), 117.
  • Lojkowska E, Masclaux C, Boccara M, Robert‐Baudouy J, Hugouvieux‐Cotte‐Pattat N (1995) Characterization of the pelL gene encoding a novel pectate lyase of Erwinia chrysanthemi 3937. Molecular Microbiology 16(6): 1183-1195.
  • 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(9): 1150-1163.
  • Mashavha ML (2013) Characterisation of Pectobacterium carotovorum subsp. brasiliense isolates causing blackleg and soft rot diseases of potato in South Africa (Doctoral dissertation, University of Pretoria).
  • Nabhan S, De Boer SH, Maiss E, Wydra, K (2012) Taxonomic relatedness between Pectobacterium carotovorum subsp. carotovorum, Pectobacterium carotovorum subsp. odoriferum and Pectobacterium carotovorum subsp. brasiliense subsp. nov. Journal of Applied Microbiology, 113(4), 904-913.
  • 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(2), 470-475.
  • Ozturk M, Aksoy HM, Potrykus M, Lojkowska E (2018) Genotypic and phenotypic variability of Pectobacterium strains causing blackleg and soft rot on potato in Turkey. European Journal of Plant Pathology, 152(1), 143-155.
  • Perombelon MC, Kelman A (1980) Ecology of the soft rot erwinias. Annual Review of Phytopathology 18(1): 361-387.
  • Pérombelon MCM (2002) Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathology 51(1): 1-12.
  • Portier P, Pédron J, Taghouti G, Fischer-Le Saux M, Caullireau E, Bertrand C., Barny MA (2019) Elevation of Pectobacterium carotovorum subsp. odoriferum to species level as Pectobacterium odoriferum sp. nov., proposal of Pectobacterium brasiliense sp. nov. and Pectobacterium actinidiae sp. nov., emended description of Pectobacterium carotovorum and description of Pectobacterium versatile sp. nov., isolated from streams and symptoms on diverse plants. International journal of systematic and evolutionary microbiology, 69(10), 3207-3216.
  • Toth IK, Van Der Wolf JM, Saddler G, Lojkowska E, Hélias, V, Pirhonen M, Elphinstone JG (2011) Dickeya species: an emerging problem for potato production in Europe. Plant pathology, 60(3), 385-399.
  • Samson R, Legendre JB, Christen R, Fischer-Le Saux M, Achouak W, Gardan L, 2005. Transfer of Pectobacterium chrysanthemi (Burkholder et al., 1953) Brenner I. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. International Journal of Systematic and Evolutionary Microbiology 55, 1415–27.
  • Sarfraz S, Sahi ST, Oulghazi S, Riaz K, Rajput NA, Atiq M, Faure D (2020) Species diversity of Dickeya and Pectobacterium causing potato blackleg disease in Pakistan. Plant disease, 104(5), 1492-1499.
  • She XM, Lan GB, Tang YF, He ZF (2017) Pectobacterium carotovorum subsp. brasiliense causing pepper black spot disease in China. Journal of Plant Pathology, 769-772.
  • Van der Wolf JM, Acuña I, De Boer SH, Brurberg MB, Cahill G, Charkowski AO, Fleming T (2021) Diseases caused by Pectobacterium and Dickeya species around the world. In Plant diseases caused by Dickeya and Pectobacterium species (pp. 215-261). Springer.
  • Voronina MV, Lukianova AA, Shneider MM, Korzhenkov AA, Toschakov SV, Miroshnikov KA, Ignatov AN (2021) First Report of Pectobacterium polaris causing soft rot and blackleg of potato in Russia. Plant Disease, PDIS-09.
  • Waleron M, Waleron K, Podhajska AJ, Łojkowska E (2002) Genotyping of bacteria belonging to the former Erwinia genus by PCR-RFLP analysis of a recA gene fragment. Microbiology 148(2): 583-595.
  • Waleron M, Waleron K, Lojkowska E (2013) Occurrence of Pectobacterium wasabiae in potato field samples. European Journal of Plant Pathology, 137(1), 149-158.
  • Waleron M, Waleron K, Lojkowska E (2014) Characterization of Pectobacterium carotovorum subsp. odoriferum causing soft rot of stored vegetables. European Journal of Plant Pathology, 139(3), 457-469.
  • Waleron M, Waleron K, Lojkowska E (2015) First report of Pectobacterium carotovorum subsp. brasiliense causing soft rot on potato and other vegetables in Poland. Plant Disease, 99(9), 1271-1271.
  • Waleron M, Misztak A, Waleron M, Jonca J, Furmaniak M, Waleron K (2019a) Pectobacterium polonicum sp. nov. isolated from vegetable fields. International journal of systematic and evolutionary microbiology, 69(6), 1751-1759.
  • Waleron M, Misztak A, Jońca J, Waleron K (2019b) First report of Pectobacterium polaris causing soft rot of potato in Poland. Plant Disease, 103(1), 144-144.
  • Wang J, Han W, Li Z, Cheng J, Pan Y, Zhao D, Zhu, J (2021) First Report of Pectobacterium polaris causing aerial stem rot of potato in China. Plant disease.
  • Zlatković N, Prokić A, Gašić K, Kuzmanović N, Ivanović M, Obradović A (2019) First report of Pectobacterium carotovorum subsp. brasiliense causing soft rot on squash and watermelon in Serbia. Plant Disease, 103(10), 2667-2667.

Bakteriyel yumuşak çürüklük hastalığına neden olan Pectobacterium polaris’in konukçu aralığının belirlenmesi

Year 2022, , 234 - 240, 01.08.2022
https://doi.org/10.37908/mkutbd.1064147

Abstract

Amaç: Pectobacterium polaris, dünyanın farklı bölgelerinde bildirilen ve yakın zamanda Türkiye’de tespit edilen Pectobacterium spp.’de yer alan yeni bir bakteriyel patojendir. Bu çalışmada P. polaris’in konukçu aralığını belirlemek için, patojenin iki ayrı izolatının farklı konukçularda patojenisitesini değerlendirmek ve etmene karşı risk altında olabilecek bitki türlerinin belirlenmesi hedeflenmiştir.

Yöntem ve Bulgular: Nevşehir ilinde karabacak hastalık belirtisi gösteren patates bitkilerinin enfekteli gövde dokusundan 2019 yılı vejetasyon döneminde izole edilmiş P. polaris (NV3 and NV19) izolatları bitkilere yapay inokulasyonlar için kullanılmıştır. İzolatların bakteriyel süspansiyonları hazırlanarak kırmızı lahana, brokoli, karnabahar, soğan, sarımsak, havuç, domates, biber, patlıcan, hıyar, kabak, kavun, karpuz, marul, ayçiçeği ve şeker pancarı bitkilerine bulaştırılmıştır. Yapay inokulasyon yapılan tüm bitkilerde meydana gelen hastalık simptomları ile P. polaris’in her iki izolatının hastalığa neden olduğu belirlenmiştir. Enfekteli bitki dokularından patojene ait koloniler yeniden izole edilmiştir.

Genel Yorum: Pectobacterium türleri, çok sayıda bitki türünde yumuşak çürüklüğe neden olan oldukça yıkıcı bakteriyel bitki patojenleridir. Dünyanın farklı bölgelerinde bildirilen ve ülkemizde oldukça yeni bir patojen olarak tanımlanan P. polaris’in geniş bir konukçu aralığında patojen olduğu belirlenmiştir. Patojenin ilk olarak izole edildiği bölgede hastalığın mücadelesine yönelik önlemler alınmalı ve özellikle patates yumruları yoluyla patojenin hastalıktan ari üretim alanlarına taşınması önlenmelidir.

Çalışmanın Önemi ve Etkisi: Testlenen tüm bitkilerin P. polaris için konukçu olduğu belirlenmiştir. Türkiye’de ekonomik öneme sahip olan bu kültür bitkilerinin patojene karşı risk durumları ilk kez bu çalışma ile belirlenmiştir.

Project Number

6602c-ZF/21-472

References

  • Agrios GN (2006) Bacterial soft rots, 5th edn. Academic Press, San Diego.
  • Aytop Y, Çukadar, M, Şahin A (2014) Agricultural sector profile of Turkey in the world. Türk Tarım ve Doğa Bilimleri Dergisi, 1(Özel Sayı-1), 688-694.
  • Cariddi C, Bubici G (2016) First report of bacterial pith soft rot caused by Pectobacterium carotovorum subsp. brasiliense on artichoke in Italy. Journal of Plant Pathology, 563-568.
  • Caruso A, Licciardello G, La Rosa R, Catara V, Bella P (2016) Mixed infection of Pectobacterium carotovorum subsp. carotovorum and P. carotovorum subsp. brasiliensis in tomato stem rot in Italy. Journal of Plant Pathology, 98(3), 661-665.
  • Charkowski AO (2007) The soft rot Erwinia. In Plant-associated bacteria (pp. 423-505). Springer, Dordrecht.
  • Chen C, Li X, Bo Z, Du W, Fu L, Tian, Y, Cui S, Shi Y, Xie H (2021) Occurrence, Characteristics, and PCR-Based Detection of Pectobacterium polaris Causing Soft Rot of Chinese Cabbage in China. Plant Disease, 105(10), 2880-2887.
  • Czajkowski R, Perombelon MC, van Veen JA, van der Wolf JM (2011) Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: a review. Plant pathology, 60(6), 999-1013.
  • Czajkowski R, Pérombelon MCM, Jafra S, Lojkowska E, Potrykus M, Van Der Wolf, JM, Sledz W (2015) Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: a review. Annals of Applied Biology 166(1): 18-38.
  • Dadaşoğlu F, Kotan R (2017) Identification and characterization of Pectobacterium carotovorum. J Anim Plant Sci, 27, 647-654.
  • De Boer SH, Li X, Ward LJ (2012) Pectobacterium spp. associated with bacterial stem rot syndrome of potato in Canada. Phytopathology 102(10): 937-947.
  • Dees MW, Lysøe E, Rossmann S, Perminow J, Brurberg MB (2017) Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology, 67(12), 5222-5229.
  • 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(3): 535-545.
  • Gardan L, Gouy C, Christen R, Samson R (2003) Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. International journal of systematic and evolutionary microbiology, 53(2), 381-391.
  • Khayi S, Cigna J, Chong TM, Quêtu-Laurent A, Chan KG, Hélias 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(12), 5379-5383.
  • Hélias V, Hamon P, Huchet E, Wolf JVD, Andrivon D (2012) Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya. Plant Pathology 61(2): 339-345.
  • Lee DH, Kim JB, Lim JA, Han SW, Heu S (2014) Genetic diversity of Pectobacterium carotovorum subsp. brasiliensis isolated in Korea. The plant pathology journal, 30(2), 117.
  • Lojkowska E, Masclaux C, Boccara M, Robert‐Baudouy J, Hugouvieux‐Cotte‐Pattat N (1995) Characterization of the pelL gene encoding a novel pectate lyase of Erwinia chrysanthemi 3937. Molecular Microbiology 16(6): 1183-1195.
  • 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(9): 1150-1163.
  • Mashavha ML (2013) Characterisation of Pectobacterium carotovorum subsp. brasiliense isolates causing blackleg and soft rot diseases of potato in South Africa (Doctoral dissertation, University of Pretoria).
  • Nabhan S, De Boer SH, Maiss E, Wydra, K (2012) Taxonomic relatedness between Pectobacterium carotovorum subsp. carotovorum, Pectobacterium carotovorum subsp. odoriferum and Pectobacterium carotovorum subsp. brasiliense subsp. nov. Journal of Applied Microbiology, 113(4), 904-913.
  • 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(2), 470-475.
  • Ozturk M, Aksoy HM, Potrykus M, Lojkowska E (2018) Genotypic and phenotypic variability of Pectobacterium strains causing blackleg and soft rot on potato in Turkey. European Journal of Plant Pathology, 152(1), 143-155.
  • Perombelon MC, Kelman A (1980) Ecology of the soft rot erwinias. Annual Review of Phytopathology 18(1): 361-387.
  • Pérombelon MCM (2002) Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathology 51(1): 1-12.
  • Portier P, Pédron J, Taghouti G, Fischer-Le Saux M, Caullireau E, Bertrand C., Barny MA (2019) Elevation of Pectobacterium carotovorum subsp. odoriferum to species level as Pectobacterium odoriferum sp. nov., proposal of Pectobacterium brasiliense sp. nov. and Pectobacterium actinidiae sp. nov., emended description of Pectobacterium carotovorum and description of Pectobacterium versatile sp. nov., isolated from streams and symptoms on diverse plants. International journal of systematic and evolutionary microbiology, 69(10), 3207-3216.
  • Toth IK, Van Der Wolf JM, Saddler G, Lojkowska E, Hélias, V, Pirhonen M, Elphinstone JG (2011) Dickeya species: an emerging problem for potato production in Europe. Plant pathology, 60(3), 385-399.
  • Samson R, Legendre JB, Christen R, Fischer-Le Saux M, Achouak W, Gardan L, 2005. Transfer of Pectobacterium chrysanthemi (Burkholder et al., 1953) Brenner I. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. International Journal of Systematic and Evolutionary Microbiology 55, 1415–27.
  • Sarfraz S, Sahi ST, Oulghazi S, Riaz K, Rajput NA, Atiq M, Faure D (2020) Species diversity of Dickeya and Pectobacterium causing potato blackleg disease in Pakistan. Plant disease, 104(5), 1492-1499.
  • She XM, Lan GB, Tang YF, He ZF (2017) Pectobacterium carotovorum subsp. brasiliense causing pepper black spot disease in China. Journal of Plant Pathology, 769-772.
  • Van der Wolf JM, Acuña I, De Boer SH, Brurberg MB, Cahill G, Charkowski AO, Fleming T (2021) Diseases caused by Pectobacterium and Dickeya species around the world. In Plant diseases caused by Dickeya and Pectobacterium species (pp. 215-261). Springer.
  • Voronina MV, Lukianova AA, Shneider MM, Korzhenkov AA, Toschakov SV, Miroshnikov KA, Ignatov AN (2021) First Report of Pectobacterium polaris causing soft rot and blackleg of potato in Russia. Plant Disease, PDIS-09.
  • Waleron M, Waleron K, Podhajska AJ, Łojkowska E (2002) Genotyping of bacteria belonging to the former Erwinia genus by PCR-RFLP analysis of a recA gene fragment. Microbiology 148(2): 583-595.
  • Waleron M, Waleron K, Lojkowska E (2013) Occurrence of Pectobacterium wasabiae in potato field samples. European Journal of Plant Pathology, 137(1), 149-158.
  • Waleron M, Waleron K, Lojkowska E (2014) Characterization of Pectobacterium carotovorum subsp. odoriferum causing soft rot of stored vegetables. European Journal of Plant Pathology, 139(3), 457-469.
  • Waleron M, Waleron K, Lojkowska E (2015) First report of Pectobacterium carotovorum subsp. brasiliense causing soft rot on potato and other vegetables in Poland. Plant Disease, 99(9), 1271-1271.
  • Waleron M, Misztak A, Waleron M, Jonca J, Furmaniak M, Waleron K (2019a) Pectobacterium polonicum sp. nov. isolated from vegetable fields. International journal of systematic and evolutionary microbiology, 69(6), 1751-1759.
  • Waleron M, Misztak A, Jońca J, Waleron K (2019b) First report of Pectobacterium polaris causing soft rot of potato in Poland. Plant Disease, 103(1), 144-144.
  • Wang J, Han W, Li Z, Cheng J, Pan Y, Zhao D, Zhu, J (2021) First Report of Pectobacterium polaris causing aerial stem rot of potato in China. Plant disease.
  • Zlatković N, Prokić A, Gašić K, Kuzmanović N, Ivanović M, Obradović A (2019) First report of Pectobacterium carotovorum subsp. brasiliense causing soft rot on squash and watermelon in Serbia. Plant Disease, 103(10), 2667-2667.
There are 39 citations in total.

Details

Primary Language English
Subjects Agricultural Engineering
Journal Section Araştırma Makalesi
Authors

Murat Ozturk 0000-0002-9677-3651

Project Number 6602c-ZF/21-472
Publication Date August 1, 2022
Submission Date February 5, 2022
Acceptance Date April 9, 2022
Published in Issue Year 2022

Cite

APA Ozturk, M. (2022). Determination of the host range of Pectobacterium polaris causing bacterial soft rot disease. Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi, 27(2), 234-240. https://doi.org/10.37908/mkutbd.1064147

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