DOI QR코드

DOI QR Code

The Rapid Apple Decline Phenomenon: Current Status and Expected Associated Factors in Korea

  • Seung-Yeol Lee (Department of Plant Medicine, Kyungpook National University) ;
  • Kari A. Peter (Department of Plant Pathology and Environmental Microbiology, Fruit Research and Extension Center, The Pennsylvania State University) ;
  • Kallol Das (Department of Plant Medicine, Kyungpook National University) ;
  • Avalos-Ruiz Diane (Department of Plant Medicine, Kyungpook National University) ;
  • Hee-Young Jung (Department of Plant Medicine, Kyungpook National University)
  • 투고 : 2023.09.25
  • 심사 : 2023.11.11
  • 발행 : 2023.12.01

초록

Rapid apple decline (RAD) is a complex phenomenon affecting cultivated apple trees and particularly dwarf rootstocks on grafted young apple trees. Since its first appearance in the United States, RAD has been reported worldwide, for example in Canada, South America, Africa, and Asia. The phenomenon has also been observed in apple orchards in Korea, and it presented similar symptoms regardless of apple cultivar and cultivation period. Most previous reports have suggested that RAD may be associated with multiple factors, including plant pathogenic infections, abiotic stresses, environmental conditions, and the susceptibility of trees to cold injury during winter. However, RAD was observed to be more severe and affect more frequently apple trees on the Malling series dwarf rootstock. In this study, we reviewed the current status of RAD worldwide and surveyed biotic and abiotic factors that are potentially closely related to it in Korea.

키워드

과제정보

This work was carried out with the support of the Cooperative Research Program for Agriculture, Science and Technology Development (Project No. RS-2020-RD009293), Rural Development Administration, Republic of Korea.

참고문헌

  1. Agnello, A. M., Breth, D. I., Tee, E. M., Cox, K. D., Villani, S. M., Ayer, K. M., Wallis, A. E., Donahue, D. J., Combs, D. B., Davis, A. E., Neal, J. A. and English-Loeb, F. M. 2017. Xylosandrus germanus (Coleoptera: Curculionidae: Scolytinae) occurrence, fungal associations, and management trials in New York apple orchards. J. Econ. Entomol. 110:2149-2164. https://doi.org/10.1093/jee/tox189
  2. Ali, S., Renderos, W., Bevis, E., Hebb, J. and Abbasi, P. A. 2020. Diaporthe eres causes stem cankers and death of young apple rootstocks in Canada. Can. J. Plant Pathol. 42:218-227. https://doi.org/10.1080/07060661.2019.1653377
  3. Avalos-Ruiz, D., Lim, G.-J., Lim, S.-K., Ten, L. N., Kang, I.-K., Lee, S.-Y. and Jung, H.-Y. 2022a. Isolation and identification of an unreported fungal species in Korea and novel ice nucleation active fungus: Fusarium diversisporum. Korean J. Mycol. 50:255-262.
  4. Avalos-Ruiz, D., Ten, L. N., Kim, C.-K., Lee, S.-Y. and Jung, H.-Y. 2022b. Isolation and identification of ice nucleation active fusarium strains from rapid apple declined trees in Korea. Plant Pathol. J. 38:403-409. https://doi.org/10.5423/PPJ.NT.04.2022.0051
  5. Azizi, R., Ghosta, Y. and Ahmadpour, A. 2020. Morphological and molecular characterization of Cytospora species involved in apple decline in Iran. Mycol. Iran. 7:205-218.
  6. Das, K., Kim, Y.-H., Yoo, J., Ten, L. N., Kang, S.-J., Kang, I.-K., Lee, S.-Y. and Jung, H.-Y. 2020. Unreported post-harvest disease of apples caused by Plenodomus collinsoniae in Korea. Korean J. Mycol. 48:511-518.
  7. Delgado-Cerrone, L., Mondino-Hintz, P. and Alaniz-Ferro, S. 2016. Botryosphariaceae species associated with stem canker, die-back and fruit rot on apple in Uruguay. Eur. J. Plant Pathol. 146:637-655. https://doi.org/10.1007/s10658-016-0949-z
  8. Diaz, G. A., Valdez, A., Halleen, F., Ferrada, E., Lolas, M. and Latorre, B. A. 2022. Characterization and pathogenicity of Diplodia, Lasiodiplodia, and Neofusicoccum species causing Botryosphaeria canker and dieback of apple trees in central Chile. Plant Dis. 106:925-937. https://doi.org/10.1094/PDIS-06-21-1291-RE
  9. Failor, K. C., Liu, H., Mechan Llontop, M. E., LeBlanc, S., Eckshtain-Levi, N., Sharma, P., Reed, A., Yang, S., Tian, L., Lefevre, C. T., Menguy, N., Du, L., Monteil, C. L. and Vinatzer, B. A. 2021. Ice nucleation in a gram-positive bacterium isolated from precipitation depends on a polyketide synthase and nonribosomal peptide synthetase. ISME J. 16:890-897. https://doi.org/10.1038/s41396-021-01140-4
  10. Fontdevila Pareta, N., Lateur, M., Steyer, S., Blouin, A. G. and Massart, S. 2022. First reports of Apple luteovirus 1, Apple rubodvirus 1 and Apple hammerhead viroid infecting apples in Belgium. New Dis. Rep. 45:e12076.
  11. Fujikawa, T., Ota, N., Sasaki, M., Nakamura, T. and Iwanami, T. 2019. Emergence of apple bacterial quick decline caused by Dickeya dadantii in Japan. J. Gen. Plant Pathol. 85:314-319. https://doi.org/10.1007/s10327-019-00852-y
  12. Ilyukhin, E., Schneider, K. and Ellouze, W. 2022. First report of Botryosphaeria dothidea causing stem canker and dieback of apple trees in Ontario, Canada. Plant Dis. 106:2994.
  13. Jabiri, S., Bahra, C., MacLean, D., Radouane, N., Barka, E. A., Bendriss Amraoui, M. and Lahlali, R. 2021. Phytopythium vexans associated with apple and pear decline in the saiss plain of Morocco. Microorganisms 9:1916.
  14. Jeon, M. J. and Cho, Y. 2015. An analysis of a winter-time temperature change and an extreme cold waves frequency in Korea. J. Clim. Change Res. 6:87-94. https://doi.org/10.15531/ksccr.2015.6.2.87
  15. Kennelly, M. M., Cazorla, F. M., de Vicente, A., Ramos, C. and Sundin, G. W. 2007. Pseudomonas syringae, diseases of fruit trees: progress toward understanding and control. Plant Dis. 91:4-17. https://doi.org/10.1094/PD-91-0004
  16. Kim, Y. S., Yun, Y. J. and Jeon, Y. 2018. First report of black rot caused by Diplodia seriata on apple. Res. Plant Dis. 24:321-327 (in Korean). https://doi.org/10.5423/RPD.2018.24.4.321
  17. Korean Society of Plant Pathology. 2023. List of Plant Diseases in Korea. URL http://genebank.rda.go.kr/plantSiteList.do [30 August 2023].
  18. Kunert, A. T., Pohlker, M. L., Tang, K., Krevert, C. S., Wieder, C., Speth, K. R., Hanson, L. E., Morris, C. E., Schmale, D. G., Poschl, U. and Frohlich-Nowoisky, J. 2019. Macromolecular fungal ice nuclei in Fusarium: effects of physical and chemical processing. Biogeosciences 16:4647-4659. https://doi.org/10.5194/bg-16-4647-2019
  19. Kweon, H.-J., Sagong, D.-H., Song, Y.-Y., Park, M.-Y., Kwon, S.-I. and Kim, M.-J. 2013. Chilling requirement for breaking of internal dormancy of main apple cultivars in Korea. Korean J. Hortic. Sci. Technol. 31:666-676.
  20. Lagzian, M., Latifi, A. M., Bassami, M. R. and Mirzaei, M. 2014. An ice nucleation protein from Fusarium acuminatum: cloning, expression, biochemical characterization and computational modeling. Biotechnol. Lett. 36:2043-2051. https://doi.org/10.1007/s10529-014-1568-4
  21. Laing, J. and Binyamin, J. 2013. Climate change effect on winter temperature and precipitation of Yellowknife, Northwest territories, Canada from 1943 to 2011. Am. J. Clim. Change 2:40682.
  22. Lee, D. H., Lee, S. W., Choi, K. H., Kim, D. A. and Uhm, J. Y. 2006. Survey on the occurrence of apple diseases in Korea from 1992 to 2000. Plant Pathol. J. 22:375-380. https://doi.org/10.5423/PPJ.2006.22.4.375
  23. Lee, D. H., Shin, H. C., Cho, R. H. and Uhm, J. Y. 2009. Reducing fungicidal spray frequency for major apple diseases by increasing the spray interval from 15 to 25 days. Plant Pathol. J. 25:270-279. https://doi.org/10.5423/PPJ.2009.25.3.270
  24. Lee, S., Cha, J.-S., Kwon, Y., Lee, Y. S., Yoo, S. E., Kim, J. H. and Kim, D. 2020a. Occurrence status of five apple virus and viroid in Korea. Res. Plant Dis. 26:95-102 (in Korean). https://doi.org/10.5423/RPD.2020.26.2.95
  25. Lee, S., Cheon, W., Kwon, H. T., Lee, Y., Kim, J., Balaraju, K. and Jeon, Y. 2023. Identification and characterization of Pseudomonas syringae pv. syringae, a causative bacterium of apple canker in Korea. Plant Pathol. J. 39:88-107. https://doi.org/10.5423/PPJ.OA.08.2022.0121
  26. Lee, S.-H., Kwon, Y., Shin, H., Kim, I.-J., Nam, S.-Y., Hong, E. Y., Kwon, S.-I., Kim, D. and Cha, J.-S. 2016. Dieback of apple tree by major soil borne diseases in Chungbuk province from 2013 to 2015. Res. Plant Dis. 22:198-201 (in Korean). https://doi.org/10.5423/RPD.2016.22.3.198
  27. Lee, S.-H., Shin, H., Chang, W.-B., Ryu, K.-Y., Kim, H. T., Cha, B. and Cha, J.-S. 2020b. Dieback reality of apple trees resulting from soil-borne fungal pathogens in South Korea from 2016 to 2019. Res. Plant Dis. 26:88-94. https://doi.org/10.5423/RPD.2020.26.2.88
  28. Lee, S.-Y., Park, S.-J., Lee, J.-J., Back, C.-G., Ten, L. N., Kang, I.-K. and Jung, H.-Y. 2017. First report of fruit rot caused by Fusarium decemcellulare in apples in Korea. Korean J. Mycol. 45:54-62.
  29. Lee, S.-Y., Ten, L. N., Back, C.-G. and Jung, H.-Y. 2021a. First report of apple decline caused by Botryosphaeria sinensis in Korea. Korean J. Mycol. 49:417-423.
  30. Lee, S.-Y., Ten, L. N., Ryu, J.-J., Kang, I.-K. and Jung, H.-Y. 2021b. Colletotrichum aenigma associated with apple bitter rot on newly bred cv. RubyS apple. Res. Plant Dis. 27:70-75. https://doi.org/10.5423/RPD.2021.27.2.70
  31. Lim, G.-J., Das, K., Noh, H.-J., Lim, S.-K., Cho, Y.-J., Lee, S.-Y., Jung, H.-Y. and Kim, S. H. 2023. First report of an apple ring rot fungus Botryosphaeria kuwatsukai in Korea. Korean J. Mycol. 51:111-120.
  32. Lim, S., Baek, D., Moon J. S., Cho, I. S., Choi, G. S., Do, Y. S., Lee, D. H. and Lee, S. H. 2019a. First report of Apple luteovirus 1 and Apple rubbery wood virus 1 on apple tree rootstocks in Korea. Plant Dis. 103:591.
  33. Lim, Y.-J., Ryu, D.-K., Kang, M. K., Jeon, Y. and Park, D. H. 2019b. Draft genome sequences of Pseudomonas syringae pv. syringae strain WSPS007 causing bacterial shoot blight on apple. Korean J. Microbiol. 55:80-82.
  34. Lindow, S. E., Arny, D. C. and Upper, C. D. 1978. Erwinia herbicola: a bacterial ice nucleus active in increasing frost injury to corn. Phytopathology 68:523-527. https://doi.org/10.1094/Phyto-68-523
  35. Liu, H., Wu, L., Nikolaeva, E., Peter, K., Liu, Z., Mollov, D., Cao, M. and Li, R. 2018. Characterization of a new apple luteovirus identified by high-throughput sequencing. Virol. J. 15:85.
  36. Lodolo, X. V., Lutz, M. C., Mondino, P., Oussett, J. and Sosa, M. C. 2022. First report of Diplodia seriata, Diplodia mutila, and Dothiorella omnivora associated with apple cankers and dieback in Rio Negro, Argentina. Plant Dis. 106:325.
  37. Ma, R., Liu, Y.-M., Yin, Y.-X. and Tian, C.-M. 2018. A canker disease of apple caused by Cytospora parasitica recorded in China. For. Pathol. 48:e12416.
  38. MacDonald, J., O'Gorman, D. T., Moffat, C., Judd, G. R., Xu, H., Sanfacon, H., Hannam, K. and Forge, T. A. 2019. Recognizing apple decline in your orchard. In: Proceedings of the Apple Decline Regional Research Users' Meeting, p. 14. Agriculture and Agri-Food Canada, Summerland, BC, Canada.
  39. Malandraki, I., Beris, D., Vassilakos, N. and Varveri, C. 2020. First report of Apple luteovirus 1 in apple trees in Greece. Plant Dis. 104:2530.
  40. Mannai, S., Horrigue-Raouani, N. and Boughalleb-M'Hamdi, N. 2018. Characterization of Fusarium species associated with apple decline in Tunisian nurseries. J. Biol. Stud. 2:14-34.
  41. Mehrabi, M., Mohammadi, G. E. and Fotouhifar, K. B. 2011. Studies on Cytospora canker disease of apple trees in Semirom region of Iran. J. Agric. Technol. 7:967-982.
  42. Moran, R. E., Sun, Y., Geng, F., Zhang, D. and Fazio, G. 2011. Cold temperature tolerance of trunk and root tissues in oneor two-year-old apple rootstocks. HortScience 46:1460-1464. https://doi.org/10.21273/HORTSCI.46.11.1460
  43. Oren, E., Palacioglu, G., Koca, G., Ozan, G. N. and Bayraktar, H. 2022. First report of Neoscytalidium dimidiatum causing branch dieback and canker on apple in Turkey. J. Plant Pathol. 104:429.
  44. Park, M. S., Kim, B.-R., Park I.-H. and Hahm, S.-S. 2018. First report of two Colletotrichum species associated with bitter rot on apple fruit in Korea-C. fructicola and C. siamense. Mycobiology 46:154-158. https://doi.org/10.1080/12298093.2018.1478220
  45. Peter, K. 2018. Sudden apple decline (SAD): The Pennsylvania Experience. URL http://www.hort.cornell.edu/expo/proceedings/2018 [30 August 2023].
  46. Pouleur, S., Richard, C., Martin, J.-G. and Antoun, H. 1992. Ice nucleation activity in Fusarium acuminatum and Fusarium avenaceum. Appl. Environ. Microbiol. 58:2960-2964. https://doi.org/10.1128/aem.58.9.2960-2964.1992
  47. Rooney-Latham, S., Tidwell, T. E., Blomquist, C. L. and Peek, K. S. 2012. First report of Neofusicoccum nonquaesitum causing branch cankers on Giant Sequoia (Sequoiadendron giganteum) in North America. Plant Dis. 96:905.
  48. Rosenberger, D. 2018. Sudden apple decline: trunk-related problems in apples. Cornell University, Ithaca, NY, USA. 4 pp.
  49. Sha, S. S., Hao, H. T., Wang, L., Wang, Z., Yan, C. C. and Feng, H. Z. 2022. First report of Diplodia mutila associated with Botryosphaeria canker and dieback of apple trees in Xinjiang, China. Plant Dis. 107:557.
  50. Singh, J., Silva, K. J. P., Fuchs, M. and Khan, A. 2019. Potential role of weather, soil and plant microbial communities in rapid decline of apple trees. PLoS ONE 14:e0213293.
  51. Sobiczewski, P. and Jones, A. L. 1992. Effect of exposure to freezing temperatures on necrosis in sweet cherry shoots inoculated with Pseudomonas syringae pv. syringae or P. s. morsprunorum. Plant Dis. 76:447-451. https://doi.org/10.1094/PD-76-0447
  52. Souli, M., Abad-Campus, P., Perez-Sierra, A., Fattouch, S., Armengol, J. and Boughalleb-M'Hamdi, N. 2014. Etiology of apple tree dieback in Tunisia and abiotic factors associated with the disease. Afr. J. Microbiol. Res. 8:2272-2281. https://doi.org/10.5897/AJMR2013.6141
  53. Stokstad, E. 2019. Rapid apple decline has researchers stumped. Science 363:1259.
  54. Weaver, D. J. 1978. Interaction of Pseudomonas syringae and freezing in bacterial canker on excised peach twigs. Phytopathology 68:1460-1463. https://doi.org/10.1094/Phyto-68-1460
  55. Westwood, M. N. and Bjornstad, H. O. 1981. Winter injury to apple cultivars as affected by growth regulators, weed control method, and rootstocks. J. Am. Soc. Hortic. Sci. 106:430-432. https://doi.org/10.21273/JASHS.106.4.430
  56. Wright, A. A., Cross, A. R. and Harper, S. J. 2020. A bushel of viruses: identification of seventeen novel putative viruses by RNA-seq in six apple trees. PLoS ONE 15:e0227669.
  57. Wright, A. A., Szostek, S. A., Beaver-Kanuya, E. and Harper, S. J. 2018. Diversity of three bunya-like viruses infecting apple. Arch. Virol. 163:3339-3343. https://doi.org/10.1007/s00705-018-3999-z
  58. Xiao, H., Hao, W., Storoschuk, G., MacDonld, J. L. and Sanfacon, H. 2022. Characterizing the virome of apple orchards affected by rapid decline in the Okanagan and Similkameen valleys of British Columbia (Canada). Pathogens 11:1231.
  59. Xu, H. and Ediger, D. 2021. Rootstocks with different vigor influenced scion-water relations and stress responses in Ambrosia apple trees (Malus domestica var. Ambrosia). Plants 10:614.
  60. Yirgu, A., Gezahgne, A., Alemu, T., Havenga, M. and Mostert, L. 2021. First report of Didymosphaeria rubi-ulmifolii associated with canker and dieback of apple trees in southern Ethiopia. Phytopathol. Mediterr. 60:229-236. https://doi.org/10.36253/phyto-12400
  61. Zhang, S., Chen, J., Ma, L., Li, E., Ji, B., Sun, C., Zhou, J.-J. and Xu, B. 2022. First report of a new disease caused by Fusarium tricinctum on apple tree in China. Plant Dis. 106:1524.