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Emerging Research Advancements to Overcome the Peach Spring Frost

  • Pandiyan Muthuramalingam (Division of Horticultural Science, Gyeongsang National University) ;
  • Rajendran Jeyasri (Department of Biotechnology, Alagappa University) ;
  • Yeonju Park (Department of GreenBio Science, Gyeongsang National University) ;
  • Seongho Lee (Division of Horticultural Science, Gyeongsang National University) ;
  • Jae Hoon Jeong (Fruit Research Division, National Institute of Horticultural & Herbal Science) ;
  • Yunji Shin (Department of GreenBio Science, Gyeongsang National University) ;
  • Jinwook Kim (Department of GreenBio Science, Gyeongsang National University) ;
  • Sangmin Jung (Division of Horticultural Science, Gyeongsang National University) ;
  • Hyunsuk Shin (Division of Horticultural Science, Gyeongsang National University)
  • Received : 2023.06.21
  • Accepted : 2023.08.31
  • Published : 2023.09.30

Abstract

The phenomena of global warming has led to an increase in the average air temperature in temperate climates. Springtime frost damage is becoming more common, and after a period of dormancy, damage to buds, blooms, and developing fruits is greater significant than damage from low winter temperatures. Peaches are a crucial crop among moderate fruits. Spring frost damage in peaches can have a negative effect on crop growth, yield, and quality. It is noteworthy that these plants have evolved defenses against spring frost damage while being exposed to a variety of low temperatures in the early spring. In this current review, recent research advancements on spring frost damage avoidance in peaches were deliberated. Additionally, adaptive mechanisms of peach, such as deacclimation and reacclimation, were emphasized. Moreover, the emerging advancements using various omics approaches revealed the peach physiology and molecular mechanisms comprehensively. Furthermore, the use of chemical products and understanding the spring frost mechanisms through the use of environmental chamber temperature stimulation and infrared thermography studies were also discussed. This review is essential groundwork and paves the way to derive and design future research for agronomists and horticulturalists to overcome the challenges of spring frost damage avoidance and crop management in these circumstances.

Keywords

Acknowledgement

This work was carried out with the support of the "Cooperative Research Program for Agricultural Science & Technology Development (Project No. PJ014950042023)" funded by the Rural Development Administration, Republic of Korea.

References

  1. Allagulova, C. R., Gimalov, F. R., Shakirova, F. M. and Vakhitov, V. A. 2003. The plant dehydrins: structure and putative functions. Biochemistry (Mosc.) 68: 945-951.  https://doi.org/10.1023/A:1026077825584
  2. Ameglio, T., Decourteix, M., Alves, G., Valentin, V., Sakr, S., Julien, J. L. et al. 2004. Temperature effects on xylem sap osmolarity in walnut trees: evidence for a vitalistic model of winter embolism repair. Tree Physiol. 24: 785-793.  https://doi.org/10.1093/treephys/24.7.785
  3. Anchordoguy, T. J., Rudolph, A. S., Carpenter, J. F. and Crowe, J. H. 1987. Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24: 324-331.  https://doi.org/10.1016/0011-2240(87)90036-8
  4. Anderson, J. V., Gesch, R. W., Jia, Y., Chao, W. S. and Horvath, D. P. 2005. Seasonal shifts in dormancy status, carbohydrate metabolism, and related gene expression in crown buds of leafy spurge. Plant Cell Environ. 28:1567-1578.  https://doi.org/10.1111/j.1365-3040.2005.01393.x
  5. Arbona, V., Manzi, M., de Ollas, C. and Gomez-Cadenas, A. 2013. Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int. J. Mol. Sci. 14: 4885-4911.  https://doi.org/10.3390/ijms14034885
  6. Arora, R. and Wisniewski, M. E. 1994. Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch). II. A 60-kilodalton bark protein in cold-acclimated tissues of peach is heat stable and related to the dehydrin family of proteins. Plant Physiol. 105: 95-101.  https://doi.org/10.1104/pp.105.1.95
  7. Arora, R., Wisniewski, M. E. and Scorza, R. 1992. Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch). 1. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissue. Plant Physiol. 99: 1562-1568.  https://doi.org/10.1104/pp.99.4.1562
  8. Artlip, T. S., Wisniewski, M. E., Arora, R. and Norelli, J. L. 2016. An apple rootstock overexpressing a peach CBF gene alters growth and flowering in the scion but does not impact cold hardiness or dormancy. Hortic. Res. 3: 16006. 
  9. Artlip, T. S., Wisniewski, M. E. and Norelli, J. L. 2014. Field evaluation of apple overexpressing a peach CBF gene confirms its effect on cold hardiness, dormancy, and growth. Environ. Exp. Bot. 106: 79-86.  https://doi.org/10.1016/j.envexpbot.2013.12.008
  10. Arus, P., Verde, I., Sosinski, B., Zhebentyayeva, T. and Abbott, A. G. 2012. The peach genome. Tree Genet. Genomes 8: 531-547.  https://doi.org/10.1007/s11295-012-0493-8
  11. Aston, J. M. and Paton, D. M. 1973. Frost room design for radiation frost studies in Eucalyptus. Aust. J. Bot. 21: 193-199.  https://doi.org/10.1071/BT9730193
  12. Bogue, R. 2013. Sensors for condition monitoring: a review of technologies and applications. Sens. Rev. 33: 295-299.  https://doi.org/10.1108/SR-05-2013-675
  13. Byrne, D. H., Raseira, M. B., Bassi, D., Piagnani, M. C., Gasic K., Reighard, G. L. et al. 2012. Peach. In: Fruit Breeding: Handbook of Plant Breeding, Vol. 8, eds. by M. L. Badenes and D. H. Byrne, pp. 505-569. Springer, New York, USA. 
  14. Calle, A. and Wunsch, A. 2020. Multiple-population QTL mapping of maturity and fruit-quality traits reveals LG4 region as a breeding target in sweet cherry (Prunus avium L.). Hortic. Res. 7: 127. 
  15. Cao, K., Zhou, Z., Wang, Q., Guo, J., Zhao, P., Zhu, G. et al. 2016. Genome-wide association study of 12 agronomic traits in peach. Nat. Commun. 7: 13246. 
  16. Ceccardi, T. L., Heath, R. L. and Ting, I. P. 1995. Low-temperature exotherm measurement using infrared thermography. HortScience 30: 140-142.  https://doi.org/10.21273/HORTSCI.30.1.140
  17. Chen, C., Okie, W. R. and Beckman, T. G. 2016. Peach fruit set and buttoning after spring frost. HortScience 51: 816-821.  https://doi.org/10.21273/HORTSCI.51.7.816
  18. Chen, R., Wang, J., Li, Y., Song, Y., Huang, M., Feng, P. et al. 2023. Quantifying the impact of frost damage during flowering on apple yield in Shaanxi province, China. Eur. J. Agron. 142: 126642. 
  19. Close, T. J. 1996. Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol. Plant. 97: 795-803.  https://doi.org/10.1111/j.1399-3054.1996.tb00546.x
  20. Close, T. J. 1997. Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol. Plant. 100: 291-296.  https://doi.org/10.1111/j.1399-3054.1997.tb04785.x
  21. Dagar, A., Friedman, H. and Lurie, S. 2010. Thaumatin-like proteins and their possible role in protection against chilling injury in peach fruit. Postharvest Biol. Technol. 57: 77-85.  https://doi.org/10.1016/j.postharvbio.2010.03.009
  22. Drogoudi, P., Kazantzis, K., Kunz, A. and Blanke, M. M. 2020. Effects of climate change on cherry production in Naoussa, Greece and Bonn, Germany: adaptation strategies. EuroMediterr. J. Environ. Integr. 5: 12. 
  23. Eccel, E., Rea, R., Caffarra, A. and Crisci, A. 2009. Risk of spring frost to apple production under future climate scenarios: the role of phenological acclimation. Int. J. Biometeorol. 53: 273-286.  https://doi.org/10.1007/s00484-009-0213-8
  24. Fan, S., Bielenberg, D. G., Zhebentyayeva, T. N., Reighard, G. L., Okie, W. R., Holland, D. et al. 2010. Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol. 185: 917-930.  https://doi.org/10.1111/j.1469-8137.2009.03119.x
  25. Food and Agriculture Organization (FAO). 2021. URL http://www.fao.org/faostat/en/#data/QC [3 August 2023]. 
  26. Frederiks, T. M., Christopher, J. T., Harvey, G. L., Sutherland, M. W. and Borrell, A. K. 2012. Current and emerging screening methods to identify post-head-emergence frost adaptation in wheat and barley. J. Exp. Bot. 63: 5405-5416.  https://doi.org/10.1093/jxb/ers215
  27. Fuller, M. P. and Wisniewski, M. 1998. The use of infrared thermal imaging in the study of ice nucleation and freezing in plants. J. Therm. Biol. 23: 81-89.  https://doi.org/10.1016/S0306-4565(98)00013-8
  28. Gonzalez-Rossia, D., Reig, C., Dovis, V., Gariglio, N. and Agusti, M. 2008. Changes in carbohydrates and nitrogen content in the bark tissues induced by artificial chilling and its relationship with dormancy bud break in Prunus sp. Sci. Hortic. 118: 275-281.  https://doi.org/10.1016/j.scienta.2008.06.011
  29. Gupta, N. and Verma, V. K. 2019. Next-generation sequencing and its application: empowering in public health beyond reality. In: Microbial Technology for the Welfare of Society, ed. by P. K. Arora, pp. 313-341. Springer, Singapore. 
  30. Gusta, L. V. and Wisniewski, M. 2013. Understanding plant cold hardiness: an opinion. Physiol. Plant. 147: 4-14.  https://doi.org/10.1111/j.1399-3054.2012.01611.x
  31. Guy, C. L., Yelenosky, G. and Sweet, H. C. 1980. Light exposure and soluble sugars in citrus frost hardiness. Fl. Sci. 43: 268-273. 
  32. Harrap, M. J. M. and Rands, S. A. 2021. Floral infrared emissivity estimates using simple tools. Plant Methods 17: 23. 
  33. Herman, E. M., Rotter, K., Premakumar, R., Elwinger, G., Bae, R., EhlerKing, L. et al. 2006. Additional freeze hardiness in wheat acquired by exposure to -3℃ is associated with extensive physiological, morphological, and molecular changes. J. Exp. Bot. 57: 3601-3618.  https://doi.org/10.1093/jxb/erl111
  34. Hernandez Mora, J. R., Micheletti, D., Bink, M., Van de Weg, E., Cantin, C., Nazzicari, N. et al. 2017. Integrated QTL detection for key breeding traits in multiple peach progenies. BMC Genomics 18: 404. 
  35. International Peach Genome Initiative, Verde, I., Abbott, A. G., Scalabrin, S., Jung, S., Shu, S. et al. 2013. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat. Genet. 45: 487-494.  https://doi.org/10.1038/ng.2586
  36. Johnson, D. E. and Howell, G. S. 1981. Factors influencing critical temperatures for spring freeze damage to developing primary shoots on Concord grapevines. Am. J. Enol. Vitic. 32: 144-149.  https://doi.org/10.5344/ajev.1981.32.2.144
  37. Juice, S. M., Fahey, T. J., Siccama, T. G., Driscoll, C. T., Denny, E. G., Eagar, C. et al. 2006. Response of sugar maple to calcium addition to northern hardwood forest. Ecology 87: 1267-1280.  https://doi.org/10.1890/0012-9658(2006)87[1267:ROSMTC]2.0.CO;2
  38. Kalberer, S. R., Leyva-Estrada, N., Krebs, S. L. and Arora, R. 2007. Frost dehardening and rehardening of floral buds of deciduous azaleas are influenced by genotypic biogeography. Environ. Exp. Bot. 59: 264-275.  https://doi.org/10.1016/j.envexpbot.2006.02.001
  39. Kalberer, S. R., Wisniewski, M. and Arora, R. 2006. Deacclimation and reacclimation of cold-hardy plants: current understanding and emerging concepts. Plant Sci. 171: 3-16.  https://doi.org/10.1016/j.plantsci.2006.02.013
  40. Kasuga, J., Arakawa, K. and Fujikawa, S. 2007. High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytol.174: 569-579.  https://doi.org/10.1111/j.1469-8137.2007.02025.x
  41. Kathpalia, R. and Bhatla, S. C. 2018. Plant mineral nutrition. In: Plant Physiology, Development and Metabolism, eds. by S. C. Bhatla and M. A. Lal, pp. 37-81. Springer, Singapore. 
  42. Kaya, O. and Kose, C. 2017. Determination of resistance to low temperatures of winter buds on lateral shoot present in Karaerik (Vitis vinifera L.) grape cultivar. Acta Physiol. Plant. 39: 209. 
  43. Khan, M. N., Siddiqui, M. H., Mohammad, F., Naeem, M. and Khan, M. M. A. 2010. Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol. Plant. 32: 121-132.  https://doi.org/10.1007/s11738-009-0387-z
  44. Kossmann, J. and Lloyd, J.R. 2000. Understanding and influencing starch biochemistry. Crit. Rev. Plant Sci. 19: 171-226.  https://doi.org/10.1080/07352680091139204
  45. Lahiri, B. B., Bagavathiappan, S., Jayakumar, T. and Philip, J. 2012. Medical applications of infrared thermography: a review. Infrared Phys. Technol. 55: 221-235.  https://doi.org/10.1016/j.infrared.2012.03.007
  46. Lam, E., Male, K. B., Chong, J. H., Leung, A. C. W. and Luong, J. H. T. 2012. Applications of functionalized and nanoparticle-modified nanocrystalline cellulose. Trends Biotechnol. 30: 283-290.  https://doi.org/10.1016/j.tibtech.2012.02.001
  47. Lamichhane, J. R. 2021. Rising risks of late-spring frosts in a changing climate. Nat. Clim. Change 11: 554-555.  https://doi.org/10.1038/s41558-021-01090-x
  48. Lee, J. H., Yu, D. J., Kim, S. J., Choi, D. and Lee, H. J. 2012. Intraspecies differences in cold hardiness, carbohydrate content and β-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiol. 32: 1533-1540.  https://doi.org/10.1093/treephys/tps102
  49. Lee, S., Jeong, J. H., Kim, S. H. and Shin, H. 2021. Freezing tolerance enhancement and thermographic observation of whole peach trees applied with cellulose nanocrystals under realistic spring frost conditions using a soil-fruit-daylit-system. Plants 10: 2301. 
  50. Li, W., Chen, Y., Ye, M., Lu, H., Wang, D. and Chen, Q. 2020. Evolutionary history of the C-repeat binding factor/dehydration-responsive element-binding 1 (CBF/DREB1) protein family in 43 plant species and characterization of CBF/DREB1 proteins in Solanum tuberosum. BMC Evol. Biol. 20: 142. 
  51. Li, Y., Tian, Q., Wang, Z., Li, J., Liu, S., Chang, R. et al. 2023. Integrated analysis of transcriptomics and metabolomics of peach under cold stress. Front. Plant Sci. 14: 1153902. 
  52. Li, Y., Wang, Z., Tian, Q., Zhou, Y., Xu, J., Chang, R. et al. 2021. Quantitative proteomic analyses on the mechanisms of cold tolerance in two peach cultivars (Prunus persica L. Batsch) based on iTRAQ. Eur. J. Hortic. Sci. 86: 308-319.  https://doi.org/10.17660/eJHS.2021/86.3.10
  53. Li, Y., Wang, L., Zhu, G., Fang, W., Cao, K., Chen, C. et al. 2016. Phenological response of peach to climate change exhibits a relatively dramatic trend in China, 1983-2012. Sci. Hortic. 209: 192-200.  https://doi.org/10.1016/j.scienta.2016.06.019
  54. Liang, L., Zhang, B., Yin, X.-R., Xu, C.-J., Sun, C.-D. and Chen, K.-S. 2013. Differential expression of the CBF gene family during postharvest cold storage and subsequent shelf-life of peach fruit. Plant Mol. Biol. Rep. 31: 1358-1367.  https://doi.org/10.1007/s11105-013-0600-5
  55. Lindow, S. E., Arny, D. C. and Upper, C. D. 1982. Bacterial ice nucleation: a factor in frost injury to plants. Plant Physiol. 70: 1084-1089.  https://doi.org/10.1104/pp.70.4.1084
  56. Liu, J. and Sherif, S. M. 2019. Combating spring frost with ethylene. Front. Plant Sci. 10: 1408. 
  57. Liu, Y., Lu, S., Liu, K., Wang, S., Huang, L. and Guo, L. 2019. Proteomics: a powerful tool to study plant responses to biotic stress. Plant Methods 15: 135. 
  58. Livingston, D. P., Tuong, T. D., Murphy, J. P., Gusta, L. V., Willick, I. and Wisniewski, M. E. 2018. High-definition infrared thermography of ice nucleation and propagation in wheat under natural frost conditions and controlled freezing. Planta 247: 791-806.  https://doi.org/10.1007/s00425-017-2823-4
  59. Lu, H., Guan, Y., He, L., Adhikari, H., Pellikka, P., Heiskanen, J. et al. 2020. Patch aggregation trends of the global climate landscape under future global warming scenario. Int. J. Climatol. 40: 2674-2685.  https://doi.org/10.1002/joc.6358
  60. Marcellos, H. 1981. A plant freezing chamber with radiative and convective energy exchange. J. Agric. Eng. Res. 26: 403-408.  https://doi.org/10.1016/0021-8634(81)90116-5
  61. Marian, C. O., Krebs, S. L. and Arora, R. 2004. Dehydrin variability among Rhododendron species: a 25-kDa dehydrin is conserved and associated with cold acclimation across diverse species. New Phytol. 161: 773-780.  https://doi.org/10.1111/j.1469-8137.2003.01001.x
  62. Mathabe, P. M. K., Belay, Z. A., Ndlovu, T. and Caleb, O. J. 2020. Progress in proteomic profiling of horticultural commodities during postharvest handling and storage: a review. Sci. Hortic. 261: 108996. 
  63. Melgoza, F. J., Kusakabe, A., Nelson, S. D. and Melgar, J. C. 2014. Exogenous applications of abscisic acid increase freeze tolerance in citrus trees. Int. J. Fruit Sci. 14: 376-387.  https://doi.org/10.1080/15538362.2014.899138
  64. Milatovic, D., Nikolic, D. and Durovic, D. 2010. Variability, heritability and correlations of some factors affecting productivity in peach. Hortic. Sci. 37: 79-87.  https://doi.org/10.17221/63/2009-HORTSCI
  65. Miura, K. and Furumoto, T. 2013. Cold signaling and cold response in plants. Int. J. Mol. Sci. 14: 5312-5337.  https://doi.org/10.3390/ijms14035312
  66. Morin, X., Ameglio, T., Ahas, R., Kurz-Besson, C., Lanta, V., Lebourgeois, F. et al. 2007. Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol. 27: 817-825.  https://doi.org/10.1093/treephys/27.6.817
  67. Muthuramalingam, P., Jeyasri, R., Kalaiyarasi, D., Pandian, S., Krishnan, S. R., Satish, L. et al. 2019. Emerging advances in computational omics tools for systems analysis of Gramineae family grass species and their abiotic stress responsive functions. In: OMICS-Based Approach Plant Biotechnology, eds. by R. Banerjee, G. V. Kumar and S. P. Jeevan Kumar, pp. 185-216. Wiley, Hoboken, NJ, USA. 
  68. Muthuramalingam, P., Shin, H., Adarshan, S., Jeyasri, R., Priya, A., Chen, J.-T. et al. 2022. Molecular insights into freezing stress in peach based on multi-omics and biotechnology: an overview. Plants 11: 812. 
  69. Nilo, R., Saffie, C., Lilley, K., Baeza-Yates, R., Cambiazo, V., CamposVargas, R. et al. 2010. Proteomic analysis of peach fruit mesocarp softening and chilling injury using difference gel electrophoresis (DIGE). BMC Genomics 11: 43. 
  70. Nilo-Poyanco, R., Moraga, C., Benedetto, G., Orellana, A. and Almeida, A. M. 2021. Shotgun proteomics of peach fruit reveals major metabolic pathways associated to ripening. BMC Genomics 22: 17. 
  71. Niu, R., Zhao, X., Wang, C. and Wang, F. 2020. Transcriptome profiling of Prunus persica branches reveals candidate genes potentially involved in freezing tolerance. Sci. Hortic. 259: 108775. 
  72. Obata, T. and Fernie, A. R. 2012. The use of metabolomics to dissect plant responses to abiotic stresses. Cell. Mol. Life Sci. 69: 3225-3243.  https://doi.org/10.1007/s00018-012-1091-5
  73. Ogundiwin, E. A., Marti, C., Forment, J., Pons, C., Granell, A., Gradziel, T. M. et al. 2008. Development of ChillPeach genomic tools and identification of cold-responsive genes in peach fruit. Plant Mol. Biol. 68: 379-397.  https://doi.org/10.1007/s11103-008-9378-5
  74. Pagter, M., Alpers, J., Erban, A., Kopka, J., Zuther, E. and Hincha, D. K. 2017. Rapid transcriptional and metabolic regulation of the deacclimation process in cold acclimated Arabidopsis thaliana. BMC Genomics 18: 731. 
  75. Pagter, M. and Arora, R. 2013. Winter survival and deacclimation of perennials under warming climate: physiological perspectives. Physiol. Plant. 147: 75-87.  https://doi.org/10.1111/j.1399-3054.2012.01650.x
  76. Pagter, M., Hausman, J.-F. and Arora, R. 2011. Deacclimation kinetics and carbohydrate changes in stem tissues of Hydrangea in response to an experimental warm spell. Plant Sci. 180: 140-148.  https://doi.org/10.1016/j.plantsci.2010.07.009
  77. Pakkish, Z. and Tabatabaienia, M. S. 2016. The use and mechanism of NO to prevent frost damage to flower of apricot. Sci. Hortic. 198: 318-325.  https://doi.org/10.1016/j.scienta.2015.12.004
  78. Park, Y. and Shin, H. 2022. Frost avoidance: sodium alginate + CaCl2 can postpone flowering of 'Kawanakajima Hakuto' peach trees. Hortic. Environ. Biotechnol. 63: 643-650.  https://doi.org/10.1007/s13580-022-00428-4
  79. Parker, J. 1963. Cold resistance in woody plants. Bot. Rev. 29: 123-201.  https://doi.org/10.1007/BF02860820
  80. Patti, G. J., Yanes, O. and Siuzdak, G. 2012. Innovation: metabolomics: the apogee of the omics trilogy. Nat. Rev. Mol. Cell Biol. 13: 263-269.  https://doi.org/10.1038/nrm3314
  81. Phillips, D. E. 1984. Environment test chamber. U.S. Patent H229.
  82. Pons, C., Marti, C., Forment, J., Crisosto, C. H., Dandekar, A. M. and Granell, A. 2014. A bulk segregant gene expression analysis of a peach population reveals components of the underlying mechanism of the fruit cold response. PLoS ONE 9: e90706. 
  83. Rademacher, W. 2015. Plant growth regulators: backgrounds and uses in plant production. J. Plant Growth Regul. 34: 845-872.  https://doi.org/10.1007/s00344-015-9541-6
  84. Rawandoozi, Z. J., Hartmann, T. P., Carpenedo, S., Gasic, K., da Silva Linge, C., Cai, L. et al. 2020. Identification and characterization of QTLs for fruit quality traits in peach through a multi-family approach. BMC Genomics 21: 522. 
  85. Raza, A., Razzaq, A., Mehmood, S. S., Zou, X., Zhang, X., Lv, Y. et al. 2019. Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8: 34. 
  86. Reddy, K. R., Hodges, H. F., Read, J. J., McKinion, J. M., Baker, J. T., Tarpley, L. et al. 2001. Soil-Plant-Atmosphere-Research (SPAR) facility: a tool for plant research and modeling. Biotronics 30: 27-50. 
  87. Renaut, J., Hausman, J.-F., Bassett, C., Artlip, T., Cauchie, H.-M., Witters, E. et al. 2008. Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genet. Genomes 4: 589-600.  https://doi.org/10.1007/s11295-008-0134-4
  88. Ribeiro, A. C., De Melo-Abreu, J. P. and Snyder, R. L. 2006. Apple orchard frost protection with wind machine operation. Agric. For. Meteorol. 141: 71-81.  https://doi.org/10.1016/j.agrformet.2006.08.019
  89. Rieger, M. 1989. Freeze protection for horticultural crops. Hortic. Rev. 11: 45-109.  https://doi.org/10.1002/9781118060841.ch3
  90. Rieger, M., Lu, S. and Duemmel, M. 1991. Frost tolerance of some peach and Japanese plum cultivars. Fruit Var. J. 45: 3-6. 
  91. Roman-Figueroa, C., Bravo, L., Paneque, M., Navia, R. and Cea, M. 2021. Chemical products for crop protection against freezing stress: a review. J. Agron. Crop Sci. 207: 391-403.  https://doi.org/10.1111/jac.12489
  92. Rowland, L. J., Ogden, E. L., Ehlenfeldt, M. K. and Vinyard, B. 2005. Cold hardiness, deacclimation kinetics, and bud development among 12 diverse blueberry genotypes under field conditions. J. Am. Soc. Hortic. Sci. 130: 508-514.  https://doi.org/10.21273/JASHS.130.4.508
  93. Salam, U., Ullah, S., Tang, Z.-H., Elateeq, A. A., Khan, Y., Khan, J. et al. 2023. Plant metabolomics: an overview of the role of primary and secondary metabolites against different environmental stress factors. Life 13: 706. 
  94. Saxe, H., Cannell, M. G. R., Johnson, O., Ryan, M. G. and Vourlitis, G. 2001. Tree and forest functioning in response to global warming. New Phytol. 149: 369-399.  https://doi.org/10.1046/j.1469-8137.2001.00057.x
  95. Schupp, J. R., Baugher, T. A., Miller, S. S., Harsh, R. M. and Lesser, K. M. 2008. Mechanical thinning of peach and apple trees reduces labor input and increases fruit size. HortTechnology 18: 660-670.  https://doi.org/10.21273/HORTTECH.18.4.660
  96. Shin, H. 2013. Changes of dehydrins, carbohydrates, and gene expressions related to cold hardiness in Prunus persica (L.) Batsch. Ph.D. thesis. Chungbuk National University, Cheongju, Korea. 141 pp. 
  97. Smith, E. D. 2019. Cold hardiness and options for the freeze protection of southern highbush blueberry. Agriculture 9: 9. 
  98. Snyder, R. L. and Davis, C. A. 2000. Principles of Frost Protection. Long Version-Quick Answer FP005. University of California, Atmospheric Science, Davis, CA, USA. 26 pp. 
  99. Speakman, J. R. and Ward, S. 1998. Infrared thermography: principles and applications. Zoology 101: 224-232. 
  100. Spiers, J. M. 1978. Effect of stage of bud development on cold injury in rabbiteye blueberry. J. Am. Soc. Hortic. Sci. 103: 452-455.  https://doi.org/10.21273/JASHS.103.4.452
  101. Stier, J. C., Filiault, D. L., Wisniewski, M. and Paulta, J. P. 2003. Visual-zation of freezing progression in turfgrass using infrared video thermography. Crop Sci. 43: 415-420.  https://doi.org/10.2135/cropsci2003.4150
  102. Szlachtowska, Z. and Rurek, M. 2023. Plant dehydrins and dehydrinlike proteins: characterization and participation in abiotic stress response. Front Plant Sci. 6: 14: 1213188. 
  103. Thomashow, M. F. 1998. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 118: 1-8.  https://doi.org/10.1104/pp.118.1.1
  104. Thomashow, M. F. 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 571-599.  https://doi.org/10.1146/annurev.arplant.50.1.571
  105. Tittarelli, A., Santiago, M., Morales, A., Meisel, L. A. and Silva, H. 2009. Isolation and functional characterization of cold-regulated promoters, by digitally identifying peach fruit cold-induced genes from a large EST dataset. BMC Plant Biol. 9: 121. 
  106. Usamentiaga, R., Venegas, P., Guerediaga, J., Vega, L., Molleda, J. and Bulnes, F. G. 2014. Infrared thermography for temperature measurement and non-destructive testing. Sensors 14: 12305-12348.  https://doi.org/10.3390/s140712305
  107. Usman, M., Farooq, M., Wakeel, A., Nawaz, A., Cheema, S. A., ur Rehman, H. et al. 2020. Nanotechnology in agriculture: current status, challenges and future opportunities. Sci. Total Environ. 721: 137778. 
  108. ValizadehKaji, B. and Nikoogoftar Sedghi, M. 2020. Enhancement of frost tolerance of almond flowers using potassium. J. Plant Nutr. 43: 2822-2832.  https://doi.org/10.1080/01904167.2020.1793179
  109. Vizoso, P., Meisel, L. A., Tittarelli, A., Latorre, M., Saba, J., Caroca, R. et al. 2009. Comparative EST transcript profiling of peach fruits under different post-harvest conditions reveals candidate genes associated with peach fruit quality. BMC Genomics 10: 423. 
  110. Wang, A., Li, J., Al-Huqail, A. A., Al-Harbi, M. S., Ali, E. F., Wang, J. et al. 2021. Mechanisms of chitosan nanoparticles in the regulation of cold stress resistance in banana plants. Nanomaterials 11: 2670. 
  111. Wang, Z., Gerstein, M. and Snyder, M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10: 57-63.  https://doi.org/10.1038/nrg2484
  112. Waraich, E. A., Ahmad, R., Halim, A. and Aziz, T. 2012. Alleviation of temperature stress by nutrient management in crop plants: a review. J. Soil Sci. Plant Nutr. 12: 221-244.  https://doi.org/10.4067/S0718-95162012000200003
  113. Webster, D. E. and Ebdon, J. S. 2005. Effects of nitrogen and potassium fertilization on perennial ryegrass cold tolerance during deacclimation in late winter and early spring. HortScience 40: 842-849.  https://doi.org/10.21273/HORTSCI.40.3.842
  114. Weiser, C. J. 1970. Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169: 1269-1278.  https://doi.org/10.1126/science.169.3952.1269
  115. Welling, A. and Palva, E. T. 2006. Molecular control of cold acclimation in trees. Physiol. Plant. 127: 167-181.  https://doi.org/10.1111/j.1399-3054.2006.00672.x
  116. Wisniewski, M., Artlip, T. and Norelli, J. 2016. Dealing with frost damage and climate change in tree fruit crops. New York Fruit Q. 24: 25-28. 
  117. Wisniewski, M., Bassett, C. and Arora, R. 2004. Distribution and partial characterization of seasonally expressed proteins in different aged shoots and roots of 'Loring' peach (Prunus persica). Tree Physiol. 24: 339-345.  https://doi.org/10.1093/treephys/24.3.339
  118. Wisniewski, M. E., Bassett, C. and Gusta, L. V. 2003. An overview of cold hardiness in woody plants: seeing the forest through the trees. HortScience 38: 952-959.  https://doi.org/10.21273/HORTSCI.38.5.952
  119. Wisniewski, M. E., Bassett, C. L., Renaut, J., Farrell, R. Jr., Tworkoski, T. and Artlip, T. S. 2006. Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol. 26: 575-584.  https://doi.org/10.1093/treephys/26.5.575
  120. Wisniewski, M., Glenn, D. M., Gusta, L. and Fuller, M. P. 2008. Using infrared thermography to study freezing in plants. HortScience 43: 1648-1651.  https://doi.org/10.21273/HORTSCI.43.6.1648
  121. Wisniewski, M., Gusta, L. and Neuner, G. 2014. Adaptive mechanisms of freeze avoidance in plants: a brief update. Environ. Exp. Bot. 99: 133-140.  https://doi.org/10.1016/j.envexpbot.2013.11.011
  122. Wisniewski, M., Lindow, S. E. and Ashworth, E. N. 1997. Observations of ice nucleation and propagation in plants using infrared video thermography. Plant Physiol. 113: 327-334.  https://doi.org/10.1104/pp.113.2.327
  123. Wisniewski, M. E., Norelli, J. L., Phillips, J. G., Artlip, T. S. and Korban, S. 2012. Using an apple microarray to characterize the CBF-regulon in transgenic 'M.26' apple trees overexpressing a peach CBF gene. In: ASHS National Conference Program, p. 45. American Society for Horticultural Science, Alexandria, VA, USA. 
  124. Wisniewski, M. E., Webb, R., Balsamo, R., Close, T. J., Yu, X.-M. and Griffith, M. 1999. Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol. Plant. 105: 600-608.  https://doi.org/10.1034/j.1399-3054.1999.105402.x
  125. Wolfe, D. W., DeGaetano, A. T., Peck, G. M., Carey, M., Ziska, L. H., LeaCox, J. et al. 2018. Unique challenges and opportunities for northeastern US crop production in a changing climate. Clim. Change 146: 231-245.  https://doi.org/10.1007/s10584-017-2109-7
  126. Wong, B. L., Baggett, K. L. and Rye, A. H. 2003. Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Can. J. Bot. 81: 780-788.  https://doi.org/10.1139/b03-079
  127. Xiao, T. and Zhou, W. 2020. The third generation sequencing: the advanced approach to genetic diseases. Transl. Pediatr. 9: 163-173.  https://doi.org/10.21037/tp.2020.03.06
  128. Xie, Z., Yang, C., Liu, S., Li, M., Gu, L., Peng, X. et al. 2022. Identification of AP2/ERF transcription factors in Tetrastigma hemsleyanum revealed the specific roles of ERF46 under cold stress. Front. Plant Sci. 13: 936602. 
  129. Xu, T., Ma, C., Aytac, Z., Hu, X., Ng, K. W., White, J. C. et al. 2020. Enhancing agrichemical delivery and seedling development with biodegradable, tunable, biopolymer-based nanofiber seed coatings. ACS Sustain. Chem. Eng. 8: 9537-9548.  https://doi.org/10.1021/acssuschemeng.0c02696
  130. Yadollahi, A. 2011. Evaluation of reduction approaches on frost damages of grapes grown in moderate cold climate. Afr. J. Agric. Res. 6: 6289-6295.  https://doi.org/10.5897/AJAR11.1036
  131. Yang, C., Duan, W., Xi, K, Ren, C., Zhu, C., Chen, K. et al. 2020. Effect of salicylic acid treatment on sensory quality, flavor-related chemicals and gene expression in peach fruit after cold storage. Postharvest Biol. Technol. 161: 111089. 
  132. Yang, Y., Saand, M. A., Huang, L., Abdelaal, W. B., Zhang, J., Wu, Y. et al. 2021. Applications of multi-omics technologies for crop improvement. Front. Plant Sci. 12: 563953. 
  133. Yang, Y., Zhang, R., Duan, X., Hu, Z., Shen, M. and Leng, P. 2019. Natural cold acclimation of Ligustrum lucidum in response to exogenous application of paclobutrazol in Beijing. Acta Physiol. Plant. 41: 15. 
  134. Yu, D. J., Jun, S. H., Park, J., Kwon, J. H. and Lee, H. J. 2020. Transcriptome analysis of genes involved in cold hardiness of peach tree (Prunus persica) shoots during cold acclimation and deacclimation. Genes 11: 611. 
  135. Zhang, X., Wang, K., Ervin, E. H., Waltz, C. and Murphy, T. 2011. Metabolic changes during cold acclimation and deacclimation in five bermudagrass varieties. 1. Proline, total amino acid, protein, and dehydrin expression. Crop Sci. 51: 838-846.  https://doi.org/10.2135/cropsci2010.06.0345
  136. Zhu, L.-Q., Zhou, J. and Zhu, S.-H. 2010. Effect of a combination of nitric oxide treatment and intermittent warming on prevention of chilling injury of 'Feicheng' peach fruit during storage. Food Chem. 121: 165-170.  https://doi.org/10.1016/j.foodchem.2009.12.025