Research Article
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Effects of cold stress on protein metabolism of certain walnut cultivars

Year 2024, Volume: 5 Issue: 1, 31 - 37, 30.04.2024
https://doi.org/10.51753/flsrt.1375108

Abstract

To investigate the effects of heat shock proteins (HSPs) on walnut (Juglans regia L.) plants under low-temperature stress, first of all, low-temperature tolerances of ten walnut cultivars (Chandler, Fernor, Franquette, Pedro, Bilecik, Kaman-I, Kaman-II, Kaman-III, Sebin, and Yalova I) were determined. One-year-old shoot samples were taken from the plants in two different periods, cold-acclimated (CA) and non-acclimated (NA), and were exposed to +5°C, -5°C, -15°C and -25°C for 12 h. Cold injury was determined by ion leakage analysis in the thawed bark tissues. According to the results of this analysis, two cultivars were determined as cold-sensitive (Chandler) and cold-tolerant (Fernor) in terms of low-temperature tolerance. To examine the effects of HSPs on cold tolerance in walnut plants, the protein profiles, the amount of total protein, and the HSPs of these two cultivars were determined. As a result of the immunoblot analysis, it was determined that 44 kDa HSP23 and 59 kDa HSP60 are responsible for low-temperature tolerance in walnut plants.

Supporting Institution

Scientific Research Projects Commission of Eskisehir Osmangazi University

Project Number

2016/23A101

References

  • Abdullah, S. N. A., Azzeme, A. M., & Yousefi, K. (2022). Fine-Tuning cold stress response through regulated cellular abundance and mechanistic actions of transcription factors. Frontiers in Plant Science, 13, 850216.
  • Aletà, N., Vilanova, A., Tomàs, E., & Guàrdia, M. (2013). Frost resistance in seven commercial walnut cultivars. VII International Walnut Symposium, Shanxi, China. 389-393.
  • Almalki, A. F. Y., Arabdin, M., & Khan, A. (2021). The role of heat shock proteins in cellular homeostasis and cell survival. Cureus, 13(9), 1-7.
  • Arora, R., & 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 Physiology, 105(1), 95-101.
  • Arora, R., Wisniewski, M. E., & Scorza, R. (1992). Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch) I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiology, 99(4), 1562-1568.
  • Bae, M. S., Cho, E. J., Choi, E. Y., & Park, O. K. (2003). Analysis of the Arabidopsis nuclear proteome and its response to cold stress. The Plant Journal, 36(5), 652-663.
  • Batool, F., Agossa, B. A., Sandhu, Z. Y., Sarwar, M. B., Hassan, S., & Rashid, B. (2022). Heat shock proteins (HSP70) gene: Plant transcriptomic oven in the hot desert. In: Kimatu J. N. (eds) Advances in Plant Defense Mechanisms (pp. 1-370). IntechOpen.
  • Bourgine, B., & Guihur, A. (2021). Heat shock signaling in land plants: From plasma membrane sensing to the transcription of small heat shock proteins. Frontiers in Plant Science, 12, 710801.
  • Casares, D., Escribá, P. V., & Rosselló, C. A. (2019). Membrane lipid composition: effect on membrane and organelle structure, function and compartmentalization and therapeutic avenues. International Journal of Molecular Sciences, 20(9), 2167-2197.
  • Charrier, G., Chuine, I., Bonhomme, M., & Améglio, T. (2018a). Assessing frost damages using dynamic models in walnut trees: exposure rather than vulnerability controls frost risks. Plant, Cell & Environment, 41 (5), 1008-1021.
  • Charrier, G., Lacointe, A., & Améglio, T. (2018b). Dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut trees Juglans regia L. Frontiers in Plant Science, 9, 410551.
  • Cui, S., Huang, F., Wang, J., Ma, X., Cheng, Y., & Liu, J. (2005). A proteomic analysis of cold stress responses in rice seedlings. Proteomics, 5(12), 3162-3172.
  • Dou, N., Li, L., Fang, Y., Fan, S., & Wu, C. (2024). Comparative physiological and transcriptome analyses of tolerant and susceptible cultivars reveal the molecular mechanism of cold tolerance in Anthurium andraeanum. International Journal of Molecular Sciences, 25(1), 250.
  • Drepper, B., Bamps, B., Gobin, A., & Van Orshoven, J. (2022). Strategies for managing spring frost risks in orchards: effectiveness and conditionality—a systematic review. Environmental Evidence, 11(1), 1-24.
  • Ergin, S., Gülen, H., Kesici, M., Turhan, E., Ipek, A., & Köksal, N. (2016). Effects of high temperature stress on enzymatic and nonenzymatic antioxidants and proteins in strawberry plants. Turkish Journal of Agriculture and Forestry, 40(6), 908-917.
  • Heberling, J. M., & Muzika, R. M. (2023). Not all temperate deciduous trees are leafless in winter: The curious case of marcescence. Ecosphere, 14(3), e4410, 1-6.
  • Hu, C., Yang, J., Qi, Z., Wu, H., Wang, B., Zou, F., ... & Liu, Q. (2022). Heat shock proteins: Biological functions, pathological roles, and therapeutic opportunities. MedComm, 3(3), e161.
  • Janni, M., Maestri, E., Gullì, M., Marmiroli, M., & Marmiroli, N. (2024). Plant responses to climate change, how global warming may impact on food security: a critical review. Frontiers in Plant Science, 14, 1297569-1297582.
  • Kerbler, S. M., & Wigge, P. A. (2023). Temperature sensing in plants. Annual Review of Plant Biology, 74, 341-366.
  • Lim, C. C., Krebs, S. L., & Arora, R. (1999). A 25-kDa dehydrin associated with genotype-and age-dependent leaf freezing-tolerance in Rhododendron: a genetic marker for cold hardiness? Theoretical and Applied Genetics, 99, 912-920.
  • McLoughlin, F., Basha, E., Fowler, M. E., Kim, M., Bordowitz, J., Katiyar-Agarwal, S., & Vierling, E. (2016). Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress. Plant Physiology, 172(2), 1221-1236.
  • Miki, Y., Takahashi, D., Kawamura, Y., & Uemura, M. (2019). Temporal proteomics of Arabidopsis plasma membrane during cold- and deacclimation. Journal of Proteomics, 197(15), 71-81.
  • Nagaraju, M., Kumar, A., Jalaja, N., Rao, D. M., & Kishor, P. B. (2021). Functional exploration of chaperonin (HSP60/10) family genes and their abiotic stress-induced expression patterns in Sorghum bicolor. Current Genomics, 22(2), 137-152.
  • NIH Image, (2024). Official Website of NIH Image Home Page, https://imagej.net/nih-image/, Last Accessed on March 20, 2024.
  • Poirier, M., Bodet, C., Ploquin, S., Saint-Joanis, B., Lacointe, A., & Améglio, T. (2004). Walnut cultivar performance of cold resistance in south central France. V International Walnut Symposium, Sorrento, Italy. 281-285.
  • Ré, M. D., Gonzalez, C., Escobar, M. R., Sossi, M. L., Valle, E. M., & Boggio, S. B. (2017). Small heat shock proteins and the postharvest chilling tolerance of tomato fruit. Physiologia Plantarum, 159(2), 148-160.
  • Renaut, J., Lutts, S., Hoffmann, L., & Hausman, J. F. (2004). Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biology, 7(01), 81-90.
  • Rezaei, M., & Rohani, A. (2023). Estimating Freezing Injury on Olive Trees: A Comparative Study of Computing Models Based on Electrolyte Leakage and Tetrazolium Tests. Agriculture, 13(6), 1137.
  • Riikonen, J., Ruhanen, H., & Luoranen, J. (2023). Impact of warm spells during late fall and winter on frost hardiness of short-day treated Norway spruce seedlings. Forest Ecology and Management, 542, 121105.
  • Shahbaz, M. (2024). Heat and Wheat: Adaptation strategies with respect to heat shock proteins and antioxidant potential; an era of climate change. International Journal of Biological Macromolecules, 256, 128379.
  • Sharma, P., Pandey, A., Malviya, R., Dey, S., Karmakar, S., & Gayen, D. (2023). Genome editing for improving nutritional quality, post-harvest shelf life and stress tolerance of fruits, vegetables, and ornamentals. Frontiers in Genome Editing, 5, 1094965- 1094984.
  • Tadić, V., Gligorević, K., Mileusnić, Z., Miodragović, R., Hajmiler, M., & Radočaj, D. (2023). Agricultural engineering technologies in the control of frost damage in permanent plantations. AgriEngineering, 5(4), 2079-2111.
  • Takahashi, D., Willick, I. R., Kasuga, J., & Livingston III, D. P. (2021). Responses of the plant cell wall to sub-zero temperatures: a brief update. Plant and Cell Physiology, 62(12), 1858-1866.
  • Taylor, N. L., Heazlewood, J. L., Day, D. A., & Millar, A. H. (2005). Differential impact of environmental stresses on the pea mitochondrial proteome. Molecular & Cellular Proteomics, 4(8), 1122-1133.
  • Tian, F., Hu, X. L., Yao, T., Yang, X., Chen, J. G., Lu, M. Z., & Zhang, J. (2021). Recent advances in the roles of HSFs and HSPs in heat stress response in woody plants. Frontiers in Plant Science, 12, 704905-704912.
  • Turhan, E., & Ergin, S. (2012). Soluble sugars and sucrose-metabolizing enzymes related to cold acclimation of sweet cherry cultivars grafted on different rootstocks. The Scientific World Journal, 2012, 1-8.
  • ul Haq, S., Khan, A., Ali, M., Khattak, A. M., Gai, W. X., Zhang, H. X., ... & Gong, Z. H. (2019). Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. International Journal of Molecular Sciences, 20(21), 5321-5352.
  • Vafadar, M., Rezaei, M., & Khadivi, A. (2024). Frost hardiness of 10 olive cultivars after natural and controlled freezing. Scientia Horticulturae, 325, 112687-112696.
  • Yang, R., Yu, G., Li, H., Li, X., & Mu, C. (2020). Overexpression of small heat shock protein LimHSP16. 45 in Arabidopsis hsp17. 6II mutant enhances tolerance to abiotic stresses. Russian Journal of Plant Physiology, 67, 231-241.
  • Yurina, N. P. (2023). Heat shock proteins in plant protection from oxidative stress. Molecular Biology, 57(6), 951-964.
  • Zhang, N., Zhao, H., Shi, J., Wu, Y., & Jiang, J. (2020). Functional characterization of class I SlHSP17. 7 gene responsible for tomato cold-stress tolerance. Plant Science, 298, 110568-110580.
  • Zinta, G., Singh, R. K., & Kumar, R. (2022). Cold adaptation strategies in plants—An emerging role of epigenetics and antifreeze proteins to engineer cold resilient plants. Frontiers in Genetics, 13, 909007.
Year 2024, Volume: 5 Issue: 1, 31 - 37, 30.04.2024
https://doi.org/10.51753/flsrt.1375108

Abstract

Project Number

2016/23A101

References

  • Abdullah, S. N. A., Azzeme, A. M., & Yousefi, K. (2022). Fine-Tuning cold stress response through regulated cellular abundance and mechanistic actions of transcription factors. Frontiers in Plant Science, 13, 850216.
  • Aletà, N., Vilanova, A., Tomàs, E., & Guàrdia, M. (2013). Frost resistance in seven commercial walnut cultivars. VII International Walnut Symposium, Shanxi, China. 389-393.
  • Almalki, A. F. Y., Arabdin, M., & Khan, A. (2021). The role of heat shock proteins in cellular homeostasis and cell survival. Cureus, 13(9), 1-7.
  • Arora, R., & 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 Physiology, 105(1), 95-101.
  • Arora, R., Wisniewski, M. E., & Scorza, R. (1992). Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch) I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiology, 99(4), 1562-1568.
  • Bae, M. S., Cho, E. J., Choi, E. Y., & Park, O. K. (2003). Analysis of the Arabidopsis nuclear proteome and its response to cold stress. The Plant Journal, 36(5), 652-663.
  • Batool, F., Agossa, B. A., Sandhu, Z. Y., Sarwar, M. B., Hassan, S., & Rashid, B. (2022). Heat shock proteins (HSP70) gene: Plant transcriptomic oven in the hot desert. In: Kimatu J. N. (eds) Advances in Plant Defense Mechanisms (pp. 1-370). IntechOpen.
  • Bourgine, B., & Guihur, A. (2021). Heat shock signaling in land plants: From plasma membrane sensing to the transcription of small heat shock proteins. Frontiers in Plant Science, 12, 710801.
  • Casares, D., Escribá, P. V., & Rosselló, C. A. (2019). Membrane lipid composition: effect on membrane and organelle structure, function and compartmentalization and therapeutic avenues. International Journal of Molecular Sciences, 20(9), 2167-2197.
  • Charrier, G., Chuine, I., Bonhomme, M., & Améglio, T. (2018a). Assessing frost damages using dynamic models in walnut trees: exposure rather than vulnerability controls frost risks. Plant, Cell & Environment, 41 (5), 1008-1021.
  • Charrier, G., Lacointe, A., & Améglio, T. (2018b). Dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut trees Juglans regia L. Frontiers in Plant Science, 9, 410551.
  • Cui, S., Huang, F., Wang, J., Ma, X., Cheng, Y., & Liu, J. (2005). A proteomic analysis of cold stress responses in rice seedlings. Proteomics, 5(12), 3162-3172.
  • Dou, N., Li, L., Fang, Y., Fan, S., & Wu, C. (2024). Comparative physiological and transcriptome analyses of tolerant and susceptible cultivars reveal the molecular mechanism of cold tolerance in Anthurium andraeanum. International Journal of Molecular Sciences, 25(1), 250.
  • Drepper, B., Bamps, B., Gobin, A., & Van Orshoven, J. (2022). Strategies for managing spring frost risks in orchards: effectiveness and conditionality—a systematic review. Environmental Evidence, 11(1), 1-24.
  • Ergin, S., Gülen, H., Kesici, M., Turhan, E., Ipek, A., & Köksal, N. (2016). Effects of high temperature stress on enzymatic and nonenzymatic antioxidants and proteins in strawberry plants. Turkish Journal of Agriculture and Forestry, 40(6), 908-917.
  • Heberling, J. M., & Muzika, R. M. (2023). Not all temperate deciduous trees are leafless in winter: The curious case of marcescence. Ecosphere, 14(3), e4410, 1-6.
  • Hu, C., Yang, J., Qi, Z., Wu, H., Wang, B., Zou, F., ... & Liu, Q. (2022). Heat shock proteins: Biological functions, pathological roles, and therapeutic opportunities. MedComm, 3(3), e161.
  • Janni, M., Maestri, E., Gullì, M., Marmiroli, M., & Marmiroli, N. (2024). Plant responses to climate change, how global warming may impact on food security: a critical review. Frontiers in Plant Science, 14, 1297569-1297582.
  • Kerbler, S. M., & Wigge, P. A. (2023). Temperature sensing in plants. Annual Review of Plant Biology, 74, 341-366.
  • Lim, C. C., Krebs, S. L., & Arora, R. (1999). A 25-kDa dehydrin associated with genotype-and age-dependent leaf freezing-tolerance in Rhododendron: a genetic marker for cold hardiness? Theoretical and Applied Genetics, 99, 912-920.
  • McLoughlin, F., Basha, E., Fowler, M. E., Kim, M., Bordowitz, J., Katiyar-Agarwal, S., & Vierling, E. (2016). Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress. Plant Physiology, 172(2), 1221-1236.
  • Miki, Y., Takahashi, D., Kawamura, Y., & Uemura, M. (2019). Temporal proteomics of Arabidopsis plasma membrane during cold- and deacclimation. Journal of Proteomics, 197(15), 71-81.
  • Nagaraju, M., Kumar, A., Jalaja, N., Rao, D. M., & Kishor, P. B. (2021). Functional exploration of chaperonin (HSP60/10) family genes and their abiotic stress-induced expression patterns in Sorghum bicolor. Current Genomics, 22(2), 137-152.
  • NIH Image, (2024). Official Website of NIH Image Home Page, https://imagej.net/nih-image/, Last Accessed on March 20, 2024.
  • Poirier, M., Bodet, C., Ploquin, S., Saint-Joanis, B., Lacointe, A., & Améglio, T. (2004). Walnut cultivar performance of cold resistance in south central France. V International Walnut Symposium, Sorrento, Italy. 281-285.
  • Ré, M. D., Gonzalez, C., Escobar, M. R., Sossi, M. L., Valle, E. M., & Boggio, S. B. (2017). Small heat shock proteins and the postharvest chilling tolerance of tomato fruit. Physiologia Plantarum, 159(2), 148-160.
  • Renaut, J., Lutts, S., Hoffmann, L., & Hausman, J. F. (2004). Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biology, 7(01), 81-90.
  • Rezaei, M., & Rohani, A. (2023). Estimating Freezing Injury on Olive Trees: A Comparative Study of Computing Models Based on Electrolyte Leakage and Tetrazolium Tests. Agriculture, 13(6), 1137.
  • Riikonen, J., Ruhanen, H., & Luoranen, J. (2023). Impact of warm spells during late fall and winter on frost hardiness of short-day treated Norway spruce seedlings. Forest Ecology and Management, 542, 121105.
  • Shahbaz, M. (2024). Heat and Wheat: Adaptation strategies with respect to heat shock proteins and antioxidant potential; an era of climate change. International Journal of Biological Macromolecules, 256, 128379.
  • Sharma, P., Pandey, A., Malviya, R., Dey, S., Karmakar, S., & Gayen, D. (2023). Genome editing for improving nutritional quality, post-harvest shelf life and stress tolerance of fruits, vegetables, and ornamentals. Frontiers in Genome Editing, 5, 1094965- 1094984.
  • Tadić, V., Gligorević, K., Mileusnić, Z., Miodragović, R., Hajmiler, M., & Radočaj, D. (2023). Agricultural engineering technologies in the control of frost damage in permanent plantations. AgriEngineering, 5(4), 2079-2111.
  • Takahashi, D., Willick, I. R., Kasuga, J., & Livingston III, D. P. (2021). Responses of the plant cell wall to sub-zero temperatures: a brief update. Plant and Cell Physiology, 62(12), 1858-1866.
  • Taylor, N. L., Heazlewood, J. L., Day, D. A., & Millar, A. H. (2005). Differential impact of environmental stresses on the pea mitochondrial proteome. Molecular & Cellular Proteomics, 4(8), 1122-1133.
  • Tian, F., Hu, X. L., Yao, T., Yang, X., Chen, J. G., Lu, M. Z., & Zhang, J. (2021). Recent advances in the roles of HSFs and HSPs in heat stress response in woody plants. Frontiers in Plant Science, 12, 704905-704912.
  • Turhan, E., & Ergin, S. (2012). Soluble sugars and sucrose-metabolizing enzymes related to cold acclimation of sweet cherry cultivars grafted on different rootstocks. The Scientific World Journal, 2012, 1-8.
  • ul Haq, S., Khan, A., Ali, M., Khattak, A. M., Gai, W. X., Zhang, H. X., ... & Gong, Z. H. (2019). Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. International Journal of Molecular Sciences, 20(21), 5321-5352.
  • Vafadar, M., Rezaei, M., & Khadivi, A. (2024). Frost hardiness of 10 olive cultivars after natural and controlled freezing. Scientia Horticulturae, 325, 112687-112696.
  • Yang, R., Yu, G., Li, H., Li, X., & Mu, C. (2020). Overexpression of small heat shock protein LimHSP16. 45 in Arabidopsis hsp17. 6II mutant enhances tolerance to abiotic stresses. Russian Journal of Plant Physiology, 67, 231-241.
  • Yurina, N. P. (2023). Heat shock proteins in plant protection from oxidative stress. Molecular Biology, 57(6), 951-964.
  • Zhang, N., Zhao, H., Shi, J., Wu, Y., & Jiang, J. (2020). Functional characterization of class I SlHSP17. 7 gene responsible for tomato cold-stress tolerance. Plant Science, 298, 110568-110580.
  • Zinta, G., Singh, R. K., & Kumar, R. (2022). Cold adaptation strategies in plants—An emerging role of epigenetics and antifreeze proteins to engineer cold resilient plants. Frontiers in Genetics, 13, 909007.
There are 42 citations in total.

Details

Primary Language English
Subjects Plant Physiology
Journal Section Research Articles
Authors

Sergül Ergin 0000-0002-7720-5536

Fırat Altıntaş 0009-0007-6799-1290

Project Number 2016/23A101
Publication Date April 30, 2024
Submission Date October 24, 2023
Acceptance Date February 11, 2024
Published in Issue Year 2024 Volume: 5 Issue: 1

Cite

APA Ergin, S., & Altıntaş, F. (2024). Effects of cold stress on protein metabolism of certain walnut cultivars. Frontiers in Life Sciences and Related Technologies, 5(1), 31-37. https://doi.org/10.51753/flsrt.1375108

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