Факторы вирулентности патогена как основа для разработки методов и стратегий борьбы с болезнью растений на примере бактериального ожога яблони (обзор)

   Актуальность. Проведен анализ отечественной и зарубежной литературы, который свидетельствует о широком распространении и вредоносности Erwinia amylovora (Burrill.) Winslow et al. − возбудителя бактериального ожога плодовых культур, в том числе яблони. Болезнь наносит значительный ущерб сельскохозяйственному производству.

   Результаты. К настоящему времени заболевание выявлено более чем в 50 странах мира. Возбудитель поражает около 200 видов семейства Rosaceae, вызывает усыхание отдельных органов с последующей гибелью всего растения. Высокий уровень вирулентности бактерии обеспечивается рядом физиологических особенностей. E. amylovora оснащена системой секреции эффекторных белков III типа, что позволяет ей доставлять их непосредственно в клетку хозяина. Также продукция экзополисахаридов, липополисахаридов, подвижность клеток и другие свойства помогают бактерии колонизировать растения-хозяева. Возможность управления данными факторами вирулентности обеспечит снижение способности бактерии вызывать ожог на плодовых культурах. С этой точки зрения перспективными являются методы борьбы с болезнью, основанные на создании условий для несовместимых взаимодействий растения-хозяина и патогена. Данный подход базируется на углубленном понимании механизма патогенеза E. amylovora. В связи с этим необходима информация о факторах вирулентности бактерии и особенностях иммунного ответа растения, ответственных за установление взаимосвязи паразита и хозяина.

   Заключение. Настоящий обзор содержит материал по ряду направлений, связанных с возбудителем бактериального ожога плодовых культур E. amylovora. Освещены вопросы географического распространения бактерии; определен круг растений-хозяев; дана биологическая характеристика E. amylovora; описаны симптомы вызываемого ею заболевания; выявлены факторы вирулентности, наиболее значимые для обеспечения защиты растений от изучаемой болезни. Рассматриваются теоретические и практические достижения в области генетики, молекулярной биологии, физиологии растений, микробиологии, которые имеют большое значение для интеграции современных биотехнологий с целью повышения эффективности борьбы с бактериальным ожогом плодовых культур.

1. Ignatov A.N., Egorova M.S., Khodykina M.V. Spread of bacterial and phytoplasma plant diseases in Russia. Plant protection and quarantine. 2015;(5):6-9. (In Russ.) https://elibrary.ru/trkkdp

2. Karimova E.V., Shneider Yu.A., Smirnova I.P., Pakina E.N., Astarkhanova T.S. Phytopathogenic bacteria Erwinia amylovora and Acidovorax citrulli and analysis of their phytosanitary risk. Development problems of regional agro-industrial complex. 2019;(4):71-77. (In Russ.) https://elibrary.ru/hwyxog

3. Drenova N.V., Kondratyev M.O., Kharchenko A.A., Tsymbal Yu.S., Sukholozova E.A., Kvashnina N.A., Dzhalilov F.S. Rowan (Sorbus spp.) as a potential host plant of the causative agent of bacterial blight of fruit crops (Erwinia amylovora) in the Russian Federation. Phytosanitary. Plant quarantine. 2020;4(4):46-64. (In Russ.) doi: 10.69536/fkr.2020.12.82.001 https://elibrary.ru/rdszjb

4. Gorovik Yu.N., Lagonenko A.L., Evtushenkov A.N., Kukharchik N.V. Evaluation of resistance of clonal apple rootstocks to bacterial blight in vitro culture. Fruit growing. 2022;30(1):34-38. (In Russ.) https://elibrary.ru/mahhjm

5. Malakhova N.P., Skiba Yu.A., Tezekbaeva B.K., Khasein A., Dmitrieva K.D., Romashkin V.N., Zharmukha-Medova G.A., Dzhumanova Zh.K., Maltseva E.R. Prevalence of Erwinia amylovora on wild and cultivated apple trees of the genus Malus spp. for the period of 2021. Eurasian Journal of Applied Biotechnology. 2022;(2):62-71. (In Russ.) doi: 10.11134/btp.2.2022.9 https://elibrary.ru/oamocs

6. Pesotskaya K. Yu., Lagonenko A. L., Evtushenkov A. N. Effect of OHRR gene deletion on the production of virulence factors by phytopathogenic bacteria Erwinia amylovora. Molecular and Applied Genetics. 2023;34:109-120. (In Russ.) https://elibrary.ru/dntxbf

7. Guliyeva Z.M. Methods for determining bacterial blight on pome crops in the western part of Azerbaijan. Bulletin of Science and Practice. 2024;10(2):105-114. doi: 10.33619/2414-2948/99/13 (In Russ.)

8. Drenova N.V. Dzhalilov F.S. Sviridova L.A. Prospects for expanding the range of host plants of the causative agent of bacterial blight of fruit crops Erwinia amylovora in the Russian Federation. Proc. of the 10^th international scientific and practical conference "Protection of plants from pests", Krasnodar. 2021:124-126 (In Russ.) https://elibrary.ru/zvyebo

9. Sadanov A.K., Suleimenova Zh.B., Ismailova E.T., Shemshura O.N., Baimakhanova B.B., Baimakhanova G.B., Bisko N.A., Molzhigitova E., Elubaeva A.E., Tleubekova D.A., Kondratiev M.O. Bacterial burn of fruit crops. Microbiology and Virology. 2023;40(1):35-46. (In Russ.) doi: 10.53729/MV-AS.2023.01.02

10. Alexandrov I.N. Bacterial blight of fruit crops in the Russian Federation. Historical background. Plant protection and quarantine. 2009;(12):26-29 (In Russ.) https://elibrary.ru/kxwfoz

11. Sobiczewski P., Iakimova E. T., Mikiciński A., Węgrzynowicz-Lesiak E., Dyki B. Necrotrophic behaviour of Erwinia amylovora in apple and tobacco leaf tissue. Plant Pathology. 2017;66(5):842-855. doi: 10.1111/ppa.12631

12. Piqué N., Miñana-Galbis D., Merino S., Tomás J. M. Virulence factors of Erwinia amylovora : a review. International journal of molecular sciences. 2015;16(6):12836-12854. doi: 10.3390/ijms160612836

13. Rezzonico F., Emeriewen O. F., Zeng Q., Peil A., Smits T. H., Sundin G. W. Burning questions for fire blight research: I. Genomics and evol.tion of Erwinia amylovora and analyses of host-pathogen interactions. Journal of Plant Pathologyю. 2024: 797-810. doi: 10.1007/s42161-023-01581-0

14. Balaž J., Radunović D., Krstić M. Status of Erwinia amylovora in Montenegro. International Symposium on Current Trends in Plant Protection with esenias workshop - Managing Invasive Alien Species in se countries: the way ahead, 25-28 septembar 2012, Beograd. 2012:373-378.

15. Evrenosoğlu Y., Misirli A., Saygili H., Bilen E., Boztepe Ö., Acarsoy, N. Evaluation of susceptibility of different pear hybrid populations to fire blight (Erwinia amylovora). Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2011;39(1):226-236.

16. Pedroncelli A., Puopolo G. This tree is on fire: a review on the ecology of Erwinia amylovora, the causal agent of fire blight disease. Journal of Plant Pathology. 2023:823-837. doi: 10.1007/s42161-023-01397-y

17. Emeriewen O.F., Wöhner T., Flachowsky H., Peil A. Malus hosts Erwinia amylovora interactions: strain pathogenicity and resistance mechanisms. Frontiers in plant science. 2019;10:551. doi: 10.3389/fpls.2019.00551

18. Yuan X., Sundin G.W., Zeng Q., Johnson K.B., Cox K.D., Yu M., Yang C.H. Erwinia amylovora type III secretion system inhibitors reduce fire blight infection under field conditions. Phytopathology®. 2023;113(12):2197-2204. doi: 10.1094/PHYTO-04-23-0111-SA

19. Mendes R.J., Luz J.P., Santos C., Tavares F. CRISPR genotyping as complementary tool for epidemiological surveillance of Erwinia amylovora outbreaks. PLoS One. 2021;16(4):e0250280. doi: 10.1371/journal.pone.0250280

20. Rezzonico F., Smits T.H.M., Duffy B. Diversity, evolution, and functionality of clustered regularly interspaced short palindromic repeat (CRISPR) regions in the fire blight pathogen Erwinia amylovora. Applied and Environmental Microbiology. 2011;77(11):3819-3829. doi: 10.1128/AEM.00177-11

21. Zeng Q., Slack S., Amine Hassani M. Pathogen Spotlight on Erwinia amylovora Recent Advances in Genomics, Resistance Breeding, and Disease Management. Phytopathology. 2023;113(12):2140-2142. doi: 10.1094/PHYTO-11-23-0439-SA

22. Klee S.M., Sinn J.P., Christian E., Holmes A.C., Zhao K., Lehman B.L., Mc Nellis T.W. Virulence genetics of an Erwinia amylovora putative polysaccharide transporter family member. Journal of bacteriology. 2020;202(22):e00390-20. doi: 10.1128/jb.00390-20

23. Kałużna M., Puławska J., Mikiciński A. Evaluation of methods for Erwinia amylovora detection. Journal of Horticultural Research. 2013;21(2):65-71. doi: 10.2478/johr-2013-0023

24. Pirc M., Ravnikar M., Tomlinson J., Dreo J. Improved fireblight diagnostics using quantitative real-time PCR detection of Erwinia amylovora chromosomal DNA. Plant Pathology. 2009;58:872-881. doi: 10.1111/j.1365-3059.2009.02083.x

25. Mager M.G. Application of diagnostic nutrient media for identification of the phytopathogen E. amylovora. Fruit and berry growing in Russia. 2013;36(2):9-15. (In Russ.) https://elibrary.ru/pwwjkl

26. Jin Y.J., Lee S.Y., Kong H.G., Yang S.I., Ham H., Lee M.H., Park D.S. Novel detection and quantification approach of Erwinia amylovora in vitro and in planta using SYBR green-based real-time PCR assay. Plant Disease. 2023;107(3):624-627. doi: 10.1094/PDIS-05-22-1227-SC

27. Brurberg M. B., Elameen A., Sletten A., Rossmann S. L. Genetic characterization of historic Norwegian Erwinia amylovora isolates by SSR-genotyping. Journal of Plant Pathology. 2024;106:987-996. doi: 10.1007/s42161-024-01596-1

28. Pesotskaya K.Yu., Lagonenko A.L., Evtushenkov A.N. Pleiotropic effect of mutation in the genes of lipopolysaccharide biosynthesis of phytopathogenic bacteria Erwinia amylovora. Molecular and Applied Genetics. 2021;30:31-38. (In Russ.) doi: 10.47612/1999-9127-2021-30-31-38 https://elibrary.ru/gbbhsy

29. Kudina I.V., Gorovik Yu.V., Lagonenko A.L., Evtushenkov A.N. Characteristics of the virulence properties of Erwinia amylovora strains. Microbial biotechnology: fundamental and applied aspects. 2018:91-98. (In Russ.) https://elibrary.ru/ihytbq

30. Baştaş K.K., Gedük A. Effected proteins in apple and Erwinia amylovora. Turkish Journal of Agriculture - Food Science and Technology. 2020;(8):215-225. doi: 10.24925/turjaf.v8isp1.215-225.3923

31. Oh C.S., Beer S.V. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiology Letters. 2005;253(2):185-192. doi: 10.1016/j.femsle.2005.09.051

32. Khan M.A., Durel C.E., Duffy B., Drouet D., Kellerhals M., Gessler C., Patocchi A. Development of molecular markers linked to the ‘Fiesta’ linkage group 7 major QTL for fire blight resistance and their application for marker-assisted selection. Genome. 2007;6(50):568-577. doi: 10.1139/G07-033

33. Kim J.F., Beer S.V. Hrp genes and harpins of Erwinia amylovora: a decade of discovery. Fire blight and its causative agent Erwinia amylovora. 2000:141-162. doi: 10.1079/9780851992945.0000

34. Castiblanco L.F., Triplett L.R., Sundin G.W. Regulation of effector delivery by type III secretion chaperone proteins in Erwinia amylovora. Frontiers in Microbiology. 2018;9:146. doi: 10.3389/fmicb.2018.00146

35. Schröpfer S., Vogt I., Broggini G.A.L., Dahl A., Richter K., Hanke M.V., Peil A. Transcriptional profile of AvrRpt2 EA-mediated resistance and susceptibility response to Erwinia amylovora in apple. Scientific reports. 2021;11(1):8685. doi: 10.1038/s41598-021-88032-x

36. Yuan X., McGhee G. C., Slack S. M., Sundin G. W. A novel signaling pathway connects thiamine biosynthesis, bacterial respiration, and production of the exopolysaccharide amylovoran in Erwinia amylovora. Molecular Plant - Microbe Interactions. 2021;34(10):1193-1208. doi: 10.1094/MPMI-04-21-0095-R

37. Carlini L., Esposito A., Ambrosino L., Bharti S., Invernizzi L. M., Piazza S., Benini S. The ams proteins and the amylovoran biosynthetic pathway: an extensive bioinformatic study. Journal of Plant Pathology. 2024;106(3):997-1010. doi: 10.1007/s42161-023-01532-9

38. Du Z., Jakovljevic V., Salm H., Geider K. Creation and genetic restoration of Erwinia amylovora strains with low levan synthesis. Physiological and molecular plant pathology. 2004;65(3):115-122. doi: 10.1016/j.pmpp.2004.12.003

39. Öner E.T., Hernández L., Combie J. Review of Levan polysaccharide: From a century of past experiences to future prospects. Biotechnology advances. 2016;34(5):827-844. doi: 10.1016/j.biotechadv.2016.05.002

40. Pesotskaya K.Yu., Lagonenko A.L., Evtushenkov A.N. Study of the role of the transcriptional regulator MARR in the virulence of phytopathogenic bacteria Erwinia amylovora. Molecular and Applied Genetics. 2021;31:53-61 (In Russ.) doi: 10.47612/1999-9127-2021-31-53-61 https://elibrary.ru/mnkzeo

41. Fontana R., Macchi G., Caproni A., Sicurella M., Buratto M., Salvatori F., Marconi P. Control of Erwinia amylovora growth by Moringa oleifera leaf extracts: In vitro and in planta effects. Plants. 2022;11(7):957. doi: 10.3390/plants11070957

42. Schachterle J.K., Gdanetz K., Pandya I., Sundin G.W.. Identification of novel virulence factors in Erwinia amylovora through temporal transcriptomic analysis of infected apple flowers under field conditions. Molecular Plant Pathology. 2022;23(6):855-869. doi: 10.1111/mpp.13199

43. Choi J.H., Kim J.Y., Park D.H. Evidence of greater competitive fitness of Erwinia amylovora over E. pyrifoliae in Korean isolates. The Plant Pathology Journal. 2022;38(4):355. doi: 10.5423/PPJ.OA.04.2022.0056

44. Polsinelli I., Borruso, L., Caliandro R., Triboli L., Esposito A., Benini S. A genome-wide analysis of desferrioxamine mediated iron uptake in Erwinia spp. reveals genes exclusive of the Rosaceae infecting strains. Scientific Reports. 2019;9(1):2818. doi: 10.1038/s41598-019-39787-x

45. Kharadi R.R., Schachterle J.K., Yuan X., Castiblanco L. F., Peng J., Slack S. M., Sundin G. W. Genetic dissection of the Erwinia amylovora disease cycle. Annual review of phytopathology. 2021;59(1):191-212. doi: 10.1146/annurev-phyto-020620-095540

46. Shafikova T.N., Omelichkina Yu.V. Molecular and genetic aspects of plant immunity to phytopathogenic bacteria and fungi. Plant Physiology. 2015;62(5):611-611. doi: 10.7868/S0015330315050140 https://elibrary.ru/udesrh

47. Shamrai S.N. Immune system of plants: basal immunity. Cytology and Genetics. 2014;48.(4):67-82.

48. He L.L., Wang X., Rothenberg D. O. N., Xu X., Wang H. H., Deng X., Cui Z. N. A novel strategy to control Pseudomonas syringae through inhibition of type III secretion system. Pesticide Biochemistry and Physiology. 2023;194:105471. doi: 10.1016/j.pestbp.2023.105471

49. Zhao Y., He S.-Y., Sundin G.W. The Erwinia amylovora avrRpt2EA gene contributes to virulence on pear and AvrRpt2EA is recognized by Arabidopsis RPS2 when expressed in Pseudomonas syringae. Molecular plant-microbe interactions. 2006;19(6):644-654. doi: 10.1094/MPMI-19-0644.

50. Lee S. Y., Kong H. G., Kang I. J., Oh H., Woo H. J., Roh E. Identification of virulence-associated genes of Erwinia amylovora by transposon mutagenesis. Korean Journal of Agricultural Science. 2023;50(2):241-247.

51. Ham H., Oh G.R., Park D.S. Genomic Data Analysis of the Nonpathogenic Erwinia amylovora Strain CP200242 Isolated from an Asian Pear Tree. PhytoFrontiers™. 2023;3(3):747-752. doi: 10.1094/PHYTOFR-12-22-0146-A

52. Pun M., Khazanov N., Galsurker O., Weitman M., Kerem Z., Senderowitz H., Yedidia I. Phloretin, an apple phytoalexin, affects the virulence and fitness of Pectobacterium brasiliense by interfering with quorum-sensing. Frontiers in Plant Science. 2021;12:671807. doi: 10.3389/fpls.2021.671807

53. Korba J., Šillerová J., Kůdela V. Resistance of apple varieties and selections to Erwinia amylovora in the Czech Republic. Plant Protection Science. 2008;44(3):91-96.

54. Emeriewen O.F., Richter K., Flachowsky H., Malnoy M., Peil A. Genetic analysis and fine mapping of the fire blight resistance locus of Malus× arnoldiana on linkage group 12 reveal first candidate genes. Frontiers in Plant Science. 2021;12:667133. doi: 10.3389/fpls.2021.667133

55. Kellerhals M., Franck L., Baumgartner I. O., Patocchi A., Frey J. E. Breeding for fire blight resistance in apple. XII International Workshop on Fire Blight. 2010:385-389. doi: 10.17660/ActaHortic.2011.896.55

56. Calenge F., Drouet D., Denancé C., Van de Weg W.E., Brisset M. N., Paulin J. P., Durel, C. E. Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theoretical and Applied Genetics. 2005;111:128-135. doi: 10.1007/s00122-005-2002-z

57. Peil A., Hanke M.-V., Flachowsky H., Garcia-Libreros T., Horner M. Bus V. Confirmation of the fire blight QTL of Malus robusta 5 on linkage group 3. Acta Hort. 2008;793:297-303. doi: 10.17660/ActaHortic.2008.793.44

58. Durel C.E., Denance C., Brisset M.N. Two distinct major QTL for resistance to fire blight co-localize on linkage group 12 in apple genotypes ‘Evereste’ and Malus floribunda clone 821. Genome. 2009;52(2):139-147. doi: 10.1139/G08-111

59. Le Roux P. M., Khan M. A., Broggini G. A., Duffy B., Gessler C., Patocchi A. Mapping of quantitative trait loci for fire blight resistance in the apple cultivars ‘Florina’ and ‘Nova Easygro’. Genome. 2010;53(9):710-722. doi: 10.1139/G10-047

60. Kairova G., Daulet N., Solomadin M., Sandybayev N., Orkara S., Beloussov V., Sapakhova Z. Identification of Apple Varieties Resistant to Fire Blight (Erwinia amylovora) Using Molecular Markers. Horticulturae. 2023;9(9):1000. doi: 10.3390/horticulturae9091000

61. Kairova G., Pozharskiy A., Daulet N., Solomadin M., Sandybayev N., Khusnitdinova M., Gritsenko D. Evaluation of Fire Blight Resistance of Eleven Apple Rootstocks Grown in Kazakhstani Fields. Applied Sciences. 2023;13(20):11530. doi: 10.3390/app132011530

62. Lyzhin A., Saveleva N. Identification of QTL FBF7 fire blight resistance in apple varieties germplasm. BIO Web of Conferences. EDP Sciences. 2021;34:02002. doi: 10.1051/bioconf/20213402002

63. Lyzhin A.S., Saveleva N.N. Occurrence of the FBF7 fire blight resistance locus in accessions of apple wild species (Malus Mill.). Proceedings on applied botany, genetics and breeding. 2023;184(4):133-142. (In Russ.) doi: 10.30901/2227-8834-2023-4-133-142 https://www.elibrary.ru/epfsmo

64. Drenova N.V., Shamshin I.N., Dubrovsky M.L. Marking QTL resistance to fire blight in apple varieties and hybrids. Fruit and Berry Growing of Russia. 2019;(59):219-226. (In Russ.) doi: 10.31676/2073-4948-2019-59-219-226 https://www.elibrary.ru/efbvwi