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Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı

Year 2023, Volume: 54 Issue: 1, 42 - 47, 31.01.2023
https://doi.org/10.5152/AUAF.2023.220608

Abstract

Sıcaklık, bitkilerin yeryüzündeki doğal yayılışının sınırlarını belirleyen iklim faktörlerindendir. Sıcaklık 0 oC’nin altına düştüğünde, bitki bünyesindeki suyun donması ile bitkide fizyolojik olayların gerçekleşmesi mümkün olmaz. Hücre içi ve hücreler arasındaki küçük buz kristalleri donma esnasında sitoplazmaya karışır ve protoplazmik yapıyı bozarak ölüme neden olur. Tabiatta iç veya dış nükleatörler tarafından başlatılan ve heterojen olarak meydana gelen donma olayında etkili olan faktörlerden bir tanesinin de bakteriler olduğu düşünülmektedir. Buz kristali oluşumunu tetikleyen (INA bakterileri) özellikle Pseudomonas syringae türüne ait bu bakterilerin asma ve diğer birçok odunsu meyve türlerinin yaşam alanlarını önemli ölçüde kısıtladığı düşünülmektedir. Bu derlemede, bağ ve bahçelerde farklı dönemlerde görülen düşük sıcaklıkların meydana getirdikleri zararlar ile bakteriler arasında bir ilişki olup olmadığı araştırılmıştır. Bu doğrultuda bakterilerin türleri, yapıları, yaşam alanları, mevsimsel popülasyon büyüklükleri, etki mekanizmaları, buz kristali oluşumunu tetiklediği sıcaklıklar, soğuk zararı ve süper soğuma ile arasındaki ilişkiler mevcut çalışmalar ışığında incelenmiş ve açıklanmaya çalışılmıştır.

References

  • Andrews, P. K., Sandidge, C. R., & Toyama, T. K. (1984). Deep supercooling of dormant and deacclimating vitis buds. American Journal of Enology and Viticulture, 35(3), 175–177.
  • Ashworth, E. N. (1986). Freezing injury in horticultural crops-research opportunities. HortScience, 21(6), 1325–1328. [CrossRef]
  • Aslantaş, R., Karakurt, H., & Karakurt, Y. (2010). Bitkilerin düşük sıcaklıklara dayanımında hücresel ve moleküler mekanizmalar. Atatürk Üniv. Ziraat Fak. Derg., 41(2), 157–167.
  • Barranco, D. N., Ruiz, N., & Gomez-del Campo, M. (2005). Frost tolerance of eight olive cultivars. Horticultural Science, 40, 558–560.
  • Bell, C. R., Dickie, G. A., Harvey, W. L. G., & Chan, J. W. Y. F. (1995). Endophytic bacteria in grapevine. Canadian Journal of Microbiology, 41(1), 46–53. [CrossRef]
  • Bradbury, J. F. (1986). Guide to plant pathogenic bacteria. CAB International: Farnham Royal, Slough.
  • Burke, J. J. (1995). Enzym adaptation to tempeaature. In N. Smirnoff (Ed.). Environment and plant metabolism: Flexibility and acclimation (pp. 63–78). Oxford, UK: Bios Scientific Publishers.
  • Centinari, M., Smith, M. S., & Londo, J. P. (2016). Assessment of freeze injury of grapevine green tissues in response to cultivars and a cryoprotectant product. HortScience, 51(7), 856–860. [CrossRef]
  • Davies, P. L. (2014). Ice-binding proteins: A remarkable diversity of structures forstopping and starting ice growth. Trends in Biochemical Sciences, 39(11), 548–555. [CrossRef]
  • Fennell, A. (2004). Freezing tolerance and injury in grapevines. Journal of Crop Improvement, 10(1–2), 201–235. [CrossRef]
  • Gardea, A. A. (1987). Freeze damage of Pinot noir (Vitis vinifera L.) as affected by bud development, INA-bacteria, and a bacterial inhibitor [Master Thesis], Oregon State University, ABD.
  • Gross, D. C., Proebsting, Jr., E. L., & Andrews, P. K. (1984). The effects of ice nucleation-active bacteria on temperatures of ice nucleation and freeze injury of Prunus flower buds at various stages of development. Journal of the American Society for Horticultural Science, 109(3), 375–380. [CrossRef]
  • Himelrick, D. G. (1991). Growth and nutritional responses of nine grape cultivars to low soil pH. HortScience, 26(3), 269–271. [CrossRef]
  • Hoose, C., & Möhler, O. (2012). Heterogeneous ice nucleation on atmospheric aerosols: A review of results from laboratory experiments. Atmospheric Chemistry and Physics, 12(20), 9817–9854. [CrossRef]
  • Itier, B., Flura, D., Brun, O., Luisetti, J., Gaignard, J. L., Choisy, C., & Lemoine, G. (1991). An analysis of sensitivity to spring frost in vine buds. Agronomie, 11(3), 169–174.
  • Jones, G. V., White, M. A., & Cooper, O. R. (2004). Climate change and global wine quality. Climatic Change, 73(3), 319–343.
  • Kappel, F. (2010). Sweet cherry cultivars vary in their susceptibility to spring frosts. HortScience, 45(1), 176–177. [CrossRef]
  • Kennelly, M. M., Cazorla, F. M., de Vicente, A., Ramos, C., & Sundin, G. W. (2007). Pseudomonas syringae diseases of fruit trees: Progress toward understanding and control. Plant Disease, 91(1), 4–17. [CrossRef]
  • Kupe, M. (2012). Küresel iklim değişikliğinin bağcılık üzerindeki etkileri. Atatürk Üniv. Ziraat Fak. Derg., 43(2), 191–196.
  • Kupe, M., & Kose, C. (2019). Determination of cold damage in field and laboratory conditions in dormant buds of Karaerik grape cultivar. Atatürk Üniv. Ziraat Fak. Derg., 50(2), 115–121.
  • Lindow, S. E. (1983). The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology, 21(1), 363–384. [CrossRef]
  • Lindow, S. E., Arny, D. C., & Upper, C. D. (1978). Distribution of ice nucleation-active bacteria on plants in nature. Applied and Environmental Microbiology, 36(6), 831–838. [CrossRef]
  • Lindow, S. E., Arny, D. C., & Upper, C. D. (1982). Bacterial ice nucleation: A factor in frost injury to plants. Plant Physiology, 70(4), 1084–1089. [CrossRef]
  • Londo, J. P., Kovaleski, A. P., & Lillis, J. A. (2018). Divergence in the transcriptional landscape between low temperature and freeze shock in cultivated grapevine (Vitis vinifera). Horticulture Research, 5(1), 10. [CrossRef]
  • Mills, L. J., Ferguson, J. C., & Keller, M. (2006). Cold-hardiness evaluation of grapevine buds and cane tissues. American Journal of Enology and Viticulture, 57(2), 194–200. [CrossRef]
  • Morris, C. E., Georgakopoulos, D. G., & Sands, D. C. (2004). Ice nucleation active bacteria and their potential role in precipitation. Journal de Physique IV, 121(5), 87–103. [CrossRef]
  • Murray, B. J., O'Sullivan, D., Atkinson, J. D., & Webb, M. E. (2012). Ice nucleation by particles immersed in supercooled cloud droplets. Chemical Society Reviews, 41(19), 6519–6554.[CrossRef]
  • Nejad, P. (2005). Pathogenic and ice-nucleation active (INA) bacteria causing dieback of willows in short rotation forestry [Doctoral Thesis]. Saint Louis University.
  • Nilsen, E. T., & Orcutt, D. M. (1996). Physiology of plants under stress. Abiotic Factors. Park, S. C., & Nakai, T. (2003). Bacteriophage control of Pseudomonas plecoglossicida infection in ayu Plecoglossus altivelis. Diseases of Aquatic Organisms, 53(1), 33–39. [CrossRef]
  • Pearce, R. S. (1988). Extracellular ice and cell shape in froststressed cereal leaves: A low temperature scanning electron microscopy study. Planta, l75(3), 13–324.
  • Pearce, R. S. (2001). Plant freezing and damage. Annals of Botany, 87(4), 417–424. [CrossRef]
  • Pinheiro, L. A. M., Pereira, C., Frazão, C., Balcão, V. M., & Almeida, A. (2019). Efficiency of phage φ6 for biocontrol of Pseudomonas syringae pv. syringae: An in vitro preliminary study. Microorganisms, 7(9), 286. [CrossRef]
  • Pouleur, S., Richard, C., Martin, J. G., & Antoun, H. (1992). Ice nucleation activity in Fusarium acuminatum and Fusarium avenaceum. Applied and Environmental Microbiology, 58(9), 2960–2964. [CrossRef]
  • Scebba, F., Sebastiani, L., & Vitagliano, C. (1998). Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiologia Plantarum, 104(4), 747–752. [CrossRef]
  • Smallwood, M., & Bowles, D. J. (2002). Plants in a cold climate. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 357(1423), 831–847. [CrossRef]
  • Smith, E. D. (2019). Cold hardiness and options for the freeze protection of southern highbush blueberry. Agriculture, 9(1), 9. [CrossRef]
  • Trought, M. C.Howell, G. S.Cherry, N. J. (1999). Practical considerations for reducing frost damage in vineyards. Report to New Zealand winegrowers reducing frost damage in vineyards Miguel de Unamuno, The Tragic Sense of Life (pp. 18-19). Lincoln University, New Zealand
  • Vali, G. (1995). Principles of ice nucleation. In R. E. Lee, G. J. Warren & L. V. Gusta (Eds.). Biological ice nucleation and its applications (p. 28). American Phytopathological Society. Warmund, M. R., & English, J. T. (1998). Ice nucleation, freezing injury, and colonization ofTotem'Strawberry flowers with ice-nucleation-active (INA) bacteria. Journal of the American Society for Horticultural Science, 123(2), 234–238. [CrossRef]
  • Warmund, M. R., Guinan, P., & Fernandez, G. (2008). Temperatures and cold damage to small fruit crops across the Eastern United States associated with the April 2007 freeze. HortScience, 43(6), 1643–1647. [CrossRef]
  • Wilson, P. W., Heneghan, A. F., & Haymet, A. D. J. (2003). Ice nucleation in nature: Supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology, 46(1), 88–98. [CrossRef]
  • Wisniewski, M., & Basett, C. (2003). An overview of cold hardiness in woody plants: Seeing the forest through the trees. Horticultural Science, 38(5), 952–954.
  • Wisniewski, M., Michael Glenn, D. M., Gusta, L., & Fuller, M. P. (2008). Using infrared thermography to study freezing in plants. HortScience, 43(6), 1648–1651. [CrossRef]
  • Research in Agricultural Sciences 2023 54(1): 42-47 l DOI: 10.5152/AUAF.2023.22060847
  • Wisniewski, M., Nassuth, A., Teulières, C., Marque, C., Rowland, J., Cao, P. B., & Brown, A. (2014). Genomics of cold hardiness in woody plants. Critical Reviews in Plant Sciences, 33(2–3), 92–24.[CrossRef]
  • Wolf, T. K. (2008). Wine grape production guide for eastern North America. Natural Resource, Agriculture and Engineering Service.
  • Yang, J. M., Meng, Q. R., Liang, Y. Q., Wang, W. F., Sun, F. Z., Zhao, T. C., Peng, W. X., & Li, S. H. (2007). Effect of ice nucleation-active bacteria on the physiology and ultrastructure of apricot floral organs. Journal of Horticultural Science and Biotechnology, 82(4), 563–570. [CrossRef]
  • Zabadal, T. J., Dami, I. E., Goffinet, M. C., Martinson, T. E., & Chien, M. L. (2007). Winter injury to grapevines and methods of protection (pp. 36–37). Michigan State University Publications on Grape Production.
  • Zhang, J., Wu, X., Niu, R., Liu, Y., Liu, N., Xu, W., & Wang, Y. (2012). Cold resistance evaluation in 25 wild grape species. Vitis, 51(4), 153–160.

Ice Nucleation Active Bacteria in Vineyards and Orchards and Low Temperature Damage

Year 2023, Volume: 54 Issue: 1, 42 - 47, 31.01.2023
https://doi.org/10.5152/AUAF.2023.220608

Abstract

Temperature is one of the climatic factors that determine the limits of the natural distribution of plants on earth. When the temperature drops below 0oC, it is not possible for physiological events to occur in the plant as the water in the plant freezes. Small ice crystals inside and between cells mix into the cytoplasm during freezing and cause death by disrupting the protoplasmic structure. Bacteria are thought to be one of the factors affecting the freezing event, which is initiated by internal or external nucleators and occurs heterogeneously in nature. These bacteria, which trigger the formation of ice crystals (INA bacteria), especially those belonging to the Pseudomonas syringae species, are thought to significantly restrict the habitats of grapevines and many other woody fruit species. In this review, it was investigated whether there is a relationship between the damage caused by low temperatures during different periods in vineyards and orchards and bacteria. In this direction, the relationships between bacteria species, structures, habitats, seasonal population sizes, mechanisms of action, temperatures triggered by ice crystal formation, cold damage, and supercooling have been examined and tried to be explained in the light of cur rent studies.

References

  • Andrews, P. K., Sandidge, C. R., & Toyama, T. K. (1984). Deep supercooling of dormant and deacclimating vitis buds. American Journal of Enology and Viticulture, 35(3), 175–177.
  • Ashworth, E. N. (1986). Freezing injury in horticultural crops-research opportunities. HortScience, 21(6), 1325–1328. [CrossRef]
  • Aslantaş, R., Karakurt, H., & Karakurt, Y. (2010). Bitkilerin düşük sıcaklıklara dayanımında hücresel ve moleküler mekanizmalar. Atatürk Üniv. Ziraat Fak. Derg., 41(2), 157–167.
  • Barranco, D. N., Ruiz, N., & Gomez-del Campo, M. (2005). Frost tolerance of eight olive cultivars. Horticultural Science, 40, 558–560.
  • Bell, C. R., Dickie, G. A., Harvey, W. L. G., & Chan, J. W. Y. F. (1995). Endophytic bacteria in grapevine. Canadian Journal of Microbiology, 41(1), 46–53. [CrossRef]
  • Bradbury, J. F. (1986). Guide to plant pathogenic bacteria. CAB International: Farnham Royal, Slough.
  • Burke, J. J. (1995). Enzym adaptation to tempeaature. In N. Smirnoff (Ed.). Environment and plant metabolism: Flexibility and acclimation (pp. 63–78). Oxford, UK: Bios Scientific Publishers.
  • Centinari, M., Smith, M. S., & Londo, J. P. (2016). Assessment of freeze injury of grapevine green tissues in response to cultivars and a cryoprotectant product. HortScience, 51(7), 856–860. [CrossRef]
  • Davies, P. L. (2014). Ice-binding proteins: A remarkable diversity of structures forstopping and starting ice growth. Trends in Biochemical Sciences, 39(11), 548–555. [CrossRef]
  • Fennell, A. (2004). Freezing tolerance and injury in grapevines. Journal of Crop Improvement, 10(1–2), 201–235. [CrossRef]
  • Gardea, A. A. (1987). Freeze damage of Pinot noir (Vitis vinifera L.) as affected by bud development, INA-bacteria, and a bacterial inhibitor [Master Thesis], Oregon State University, ABD.
  • Gross, D. C., Proebsting, Jr., E. L., & Andrews, P. K. (1984). The effects of ice nucleation-active bacteria on temperatures of ice nucleation and freeze injury of Prunus flower buds at various stages of development. Journal of the American Society for Horticultural Science, 109(3), 375–380. [CrossRef]
  • Himelrick, D. G. (1991). Growth and nutritional responses of nine grape cultivars to low soil pH. HortScience, 26(3), 269–271. [CrossRef]
  • Hoose, C., & Möhler, O. (2012). Heterogeneous ice nucleation on atmospheric aerosols: A review of results from laboratory experiments. Atmospheric Chemistry and Physics, 12(20), 9817–9854. [CrossRef]
  • Itier, B., Flura, D., Brun, O., Luisetti, J., Gaignard, J. L., Choisy, C., & Lemoine, G. (1991). An analysis of sensitivity to spring frost in vine buds. Agronomie, 11(3), 169–174.
  • Jones, G. V., White, M. A., & Cooper, O. R. (2004). Climate change and global wine quality. Climatic Change, 73(3), 319–343.
  • Kappel, F. (2010). Sweet cherry cultivars vary in their susceptibility to spring frosts. HortScience, 45(1), 176–177. [CrossRef]
  • Kennelly, M. M., Cazorla, F. M., de Vicente, A., Ramos, C., & Sundin, G. W. (2007). Pseudomonas syringae diseases of fruit trees: Progress toward understanding and control. Plant Disease, 91(1), 4–17. [CrossRef]
  • Kupe, M. (2012). Küresel iklim değişikliğinin bağcılık üzerindeki etkileri. Atatürk Üniv. Ziraat Fak. Derg., 43(2), 191–196.
  • Kupe, M., & Kose, C. (2019). Determination of cold damage in field and laboratory conditions in dormant buds of Karaerik grape cultivar. Atatürk Üniv. Ziraat Fak. Derg., 50(2), 115–121.
  • Lindow, S. E. (1983). The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology, 21(1), 363–384. [CrossRef]
  • Lindow, S. E., Arny, D. C., & Upper, C. D. (1978). Distribution of ice nucleation-active bacteria on plants in nature. Applied and Environmental Microbiology, 36(6), 831–838. [CrossRef]
  • Lindow, S. E., Arny, D. C., & Upper, C. D. (1982). Bacterial ice nucleation: A factor in frost injury to plants. Plant Physiology, 70(4), 1084–1089. [CrossRef]
  • Londo, J. P., Kovaleski, A. P., & Lillis, J. A. (2018). Divergence in the transcriptional landscape between low temperature and freeze shock in cultivated grapevine (Vitis vinifera). Horticulture Research, 5(1), 10. [CrossRef]
  • Mills, L. J., Ferguson, J. C., & Keller, M. (2006). Cold-hardiness evaluation of grapevine buds and cane tissues. American Journal of Enology and Viticulture, 57(2), 194–200. [CrossRef]
  • Morris, C. E., Georgakopoulos, D. G., & Sands, D. C. (2004). Ice nucleation active bacteria and their potential role in precipitation. Journal de Physique IV, 121(5), 87–103. [CrossRef]
  • Murray, B. J., O'Sullivan, D., Atkinson, J. D., & Webb, M. E. (2012). Ice nucleation by particles immersed in supercooled cloud droplets. Chemical Society Reviews, 41(19), 6519–6554.[CrossRef]
  • Nejad, P. (2005). Pathogenic and ice-nucleation active (INA) bacteria causing dieback of willows in short rotation forestry [Doctoral Thesis]. Saint Louis University.
  • Nilsen, E. T., & Orcutt, D. M. (1996). Physiology of plants under stress. Abiotic Factors. Park, S. C., & Nakai, T. (2003). Bacteriophage control of Pseudomonas plecoglossicida infection in ayu Plecoglossus altivelis. Diseases of Aquatic Organisms, 53(1), 33–39. [CrossRef]
  • Pearce, R. S. (1988). Extracellular ice and cell shape in froststressed cereal leaves: A low temperature scanning electron microscopy study. Planta, l75(3), 13–324.
  • Pearce, R. S. (2001). Plant freezing and damage. Annals of Botany, 87(4), 417–424. [CrossRef]
  • Pinheiro, L. A. M., Pereira, C., Frazão, C., Balcão, V. M., & Almeida, A. (2019). Efficiency of phage φ6 for biocontrol of Pseudomonas syringae pv. syringae: An in vitro preliminary study. Microorganisms, 7(9), 286. [CrossRef]
  • Pouleur, S., Richard, C., Martin, J. G., & Antoun, H. (1992). Ice nucleation activity in Fusarium acuminatum and Fusarium avenaceum. Applied and Environmental Microbiology, 58(9), 2960–2964. [CrossRef]
  • Scebba, F., Sebastiani, L., & Vitagliano, C. (1998). Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiologia Plantarum, 104(4), 747–752. [CrossRef]
  • Smallwood, M., & Bowles, D. J. (2002). Plants in a cold climate. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 357(1423), 831–847. [CrossRef]
  • Smith, E. D. (2019). Cold hardiness and options for the freeze protection of southern highbush blueberry. Agriculture, 9(1), 9. [CrossRef]
  • Trought, M. C.Howell, G. S.Cherry, N. J. (1999). Practical considerations for reducing frost damage in vineyards. Report to New Zealand winegrowers reducing frost damage in vineyards Miguel de Unamuno, The Tragic Sense of Life (pp. 18-19). Lincoln University, New Zealand
  • Vali, G. (1995). Principles of ice nucleation. In R. E. Lee, G. J. Warren & L. V. Gusta (Eds.). Biological ice nucleation and its applications (p. 28). American Phytopathological Society. Warmund, M. R., & English, J. T. (1998). Ice nucleation, freezing injury, and colonization ofTotem'Strawberry flowers with ice-nucleation-active (INA) bacteria. Journal of the American Society for Horticultural Science, 123(2), 234–238. [CrossRef]
  • Warmund, M. R., Guinan, P., & Fernandez, G. (2008). Temperatures and cold damage to small fruit crops across the Eastern United States associated with the April 2007 freeze. HortScience, 43(6), 1643–1647. [CrossRef]
  • Wilson, P. W., Heneghan, A. F., & Haymet, A. D. J. (2003). Ice nucleation in nature: Supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology, 46(1), 88–98. [CrossRef]
  • Wisniewski, M., & Basett, C. (2003). An overview of cold hardiness in woody plants: Seeing the forest through the trees. Horticultural Science, 38(5), 952–954.
  • Wisniewski, M., Michael Glenn, D. M., Gusta, L., & Fuller, M. P. (2008). Using infrared thermography to study freezing in plants. HortScience, 43(6), 1648–1651. [CrossRef]
  • Research in Agricultural Sciences 2023 54(1): 42-47 l DOI: 10.5152/AUAF.2023.22060847
  • Wisniewski, M., Nassuth, A., Teulières, C., Marque, C., Rowland, J., Cao, P. B., & Brown, A. (2014). Genomics of cold hardiness in woody plants. Critical Reviews in Plant Sciences, 33(2–3), 92–24.[CrossRef]
  • Wolf, T. K. (2008). Wine grape production guide for eastern North America. Natural Resource, Agriculture and Engineering Service.
  • Yang, J. M., Meng, Q. R., Liang, Y. Q., Wang, W. F., Sun, F. Z., Zhao, T. C., Peng, W. X., & Li, S. H. (2007). Effect of ice nucleation-active bacteria on the physiology and ultrastructure of apricot floral organs. Journal of Horticultural Science and Biotechnology, 82(4), 563–570. [CrossRef]
  • Zabadal, T. J., Dami, I. E., Goffinet, M. C., Martinson, T. E., & Chien, M. L. (2007). Winter injury to grapevines and methods of protection (pp. 36–37). Michigan State University Publications on Grape Production.
  • Zhang, J., Wu, X., Niu, R., Liu, Y., Liu, N., Xu, W., & Wang, Y. (2012). Cold resistance evaluation in 25 wild grape species. Vitis, 51(4), 153–160.
There are 48 citations in total.

Details

Primary Language Turkish
Journal Section DERLEMELER
Authors

Muhammed Küpe This is me 0000-0002-7225-8065

Publication Date January 31, 2023
Published in Issue Year 2023 Volume: 54 Issue: 1

Cite

APA Küpe, M. (2023). Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 54(1), 42-47. https://doi.org/10.5152/AUAF.2023.220608
AMA Küpe M. Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi. January 2023;54(1):42-47. doi:10.5152/AUAF.2023.220608
Chicago Küpe, Muhammed. “Üzüm Bağlarında Ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler Ve Düşük Sıcaklık Zararı”. Atatürk Üniversitesi Ziraat Fakültesi Dergisi 54, no. 1 (January 2023): 42-47. https://doi.org/10.5152/AUAF.2023.220608.
EndNote Küpe M (January 1, 2023) Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi 54 1 42–47.
IEEE M. Küpe, “Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı”, Atatürk Üniversitesi Ziraat Fakültesi Dergisi, vol. 54, no. 1, pp. 42–47, 2023, doi: 10.5152/AUAF.2023.220608.
ISNAD Küpe, Muhammed. “Üzüm Bağlarında Ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler Ve Düşük Sıcaklık Zararı”. Atatürk Üniversitesi Ziraat Fakültesi Dergisi 54/1 (January 2023), 42-47. https://doi.org/10.5152/AUAF.2023.220608.
JAMA Küpe M. Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi. 2023;54:42–47.
MLA Küpe, Muhammed. “Üzüm Bağlarında Ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler Ve Düşük Sıcaklık Zararı”. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, vol. 54, no. 1, 2023, pp. 42-47, doi:10.5152/AUAF.2023.220608.
Vancouver Küpe M. Üzüm Bağlarında ve Meyve Bahçelerinde Buz Çekirdeği Oluşumunu Tetikleyen Bakteriler ve Düşük Sıcaklık Zararı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi. 2023;54(1):42-7.

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