Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Induced freezing tolerance and free amino acids perturbation of spinach by exogenous proline

  • Shin, Hyunsuk (Department of Horticulture, Gyeongnam National University of Science and Technology) ;
  • Oh, Sewon (Department of Horticulture, Chungbuk National University) ;
  • Kim, Daeil (Department of Horticulture, Chungbuk National University) ;
  • Hong, Jeum Kyu (Department of Horticulture, Gyeongnam National University of Science and Technology) ;
  • Yun, Jae Gil (Department of Horticulture, Gyeongnam National University of Science and Technology) ;
  • Lee, Sang Woo (Department of Horticulture, Gyeongnam National University of Science and Technology) ;
  • Son, Ki-Ho (Department of Horticulture, Gyeongnam National University of Science and Technology)
  • Received : 2018.12.17
  • Accepted : 2018.12.17
  • Published : 2018.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

The objective of this study was to investigate whether exogenous proline (Pro) could confer freezing tolerance of spinach and determine fluctuations of free amino acids in spinach leaf tissues under freeze-induced stress. Treatment with Pro (10 mM) resulted in more accumulation of Pro (~2.6-fold) in Pro-treated spinaches compared to untreated ones. These Pro-pretreated spinaches were more freezing-tolerant, showing more turgid leaves and petioles compared to untreated controls. However, when spinaches pre-treated with or without Pro were subjected to freezing, there was no significant difference in overall amino acid contents, emphasizing the role of Pro as an osmoprotectant. Freezing stress prompted intensification of total amino acid contents irrespective of pretreatment with Pro. Asp, Glu, Ala, and Val were the most abundant free amino acids due to increased protein degradation and nitrogen mobilization for plant survival under freezing stress. Arg, a precursor for the synthesis of polyamines in plants, was profoundly enhanced under freezing stress. This implies that Arg plays an important role in modulating freezing tolerance. Gly, Leu, and Ile were maintained at relatively low levels in all treatments. However, Ser, Tyr, and Lys as primary constituents of dehydrins were accumulated under freezing stress, suggesting that they might play a role in increasing cryoprotective activity under freezing stress.

Keywords

References

  1. Ahmed CB, Rouina BB, Sensoy S, Boukhriss M, Abdullah FB (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58:4216-4222 https://doi.org/10.1021/jf9041479
  2. Allagulova CR, Gimalov FR, Shakirova FM, Vakhitov VA (2003) The plant dehydrins: structure and putative functions. Biochemistry (Moscow) 68:945-951 https://doi.org/10.1023/A:1026077825584
  3. Arora R (2013) Physiological study of the components of winter-hardiness in Rhododendron: cold acclimation, deacclimation kinetics, and reacclimation ability. Acta Hortic 990:67-81
  4. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206-216 https://doi.org/10.1016/j.envexpbot.2005.12.006
  5. Bagdi DL, Shaw BP (2013) Analysis of proline metabolic enzymes in Oryza sativa under NaCl stress. J Environ Biol 34:677-681
  6. Brauc S, de Vooght E, Claeys M, Geuns JMC, Hofte M, Angenon G (2012) Overexpression of arginase in Arabidopsis thaliana influences defence responses against Botrytis cinerea. Plant Biol 14:39-45 https://doi.org/10.1111/j.1438-8677.2011.00520.x
  7. Chen K, Arora R (2014) Understanding the cellular mechanism of recovery from freeze-thaw injury in spinach: possible role of aquaporins, heat shock proteins, dehydrin and antioxidant system. Physiol Plant 150:374-387 https://doi.org/10.1111/ppl.12090
  8. Chu, TM, Aspinall D, Paleg LG (1974) Stress metabolism. VI. Temperature stress and the accumulation of proline in barley and radish. Aust J Plant Physiol 1:87-97
  9. Delauney AJ, Hu CAA, Kavi Kishor PB, Verma DPS (1993) Cloning of ornithine ${\delta}$-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268:18673-18678
  10. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215-223 https://doi.org/10.1046/j.1365-313X.1993.04020215.x
  11. Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455-463 https://doi.org/10.1046/j.1469-8137.2003.00770.x
  12. Duncan DR, Widholm JM (1987) Proline accumulation and its implication in cold tolerance of regenerable maize callus. Plant Physiol 83:703-708 https://doi.org/10.1104/pp.83.3.703
  13. Fischer W-N, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188-195 https://doi.org/10.1016/S1360-1385(98)01231-X
  14. Flores T, Todd CD, Tovar-Mendez A, Dhanoa PK, Correa-Aragunde N, Hoyos ME, Brownfield DM, Mullen RT, Lamattina L, et al (2008) Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development. Plant Physiol 147:1936-1946 https://doi.org/10.1104/pp.108.121459
  15. Hanower P, Brzozowska J (1975) Effects of osmotic stress on composition of free amino acids in cotton leaves. Phytochemistry 14:1691-1694 https://doi.org/10.1016/0031-9422(75)85275-7
  16. Heuer B (2003) Influence of exogenous application of proline and glycinebetaine on growth of salt-stressed tomato plants. Plant Sci 165:693-699 https://doi.org/10.1016/S0168-9452(03)00222-X
  17. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. 2nd ed. Circular, California Agricultural Experiment Station, p 347
  18. Hoque MA, Okuma E, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553-561 https://doi.org/10.1016/j.jplph.2006.03.010
  19. Hur J, Jung KH, Lee CH, An G (2004) Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Sci 167:417-426 https://doi.org/10.1016/j.plantsci.2004.04.009
  20. Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587-1597 https://doi.org/10.1016/j.jplph.2009.04.002
  21. Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300-311 https://doi.org/10.1111/pce.12157
  22. Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 84:692-695 https://doi.org/10.1104/pp.84.3.692
  23. Lea PJ, Robinson SA, Stewart GR (1990) The enzymology and metabolism of glutamine, glutamate and asparagine. In Miflin BJ, ed, The biochemistry of plants. Academic Press, New York, USA, pp 121-169
  24. Lee TM, Chang YC (1999) An increase of ornithine ${\delta}$-aminotransferase-mediated proline synthesis in relation to high-temperature injury in Gracilaria tenuistipitata (Gigartinales, Rhodophyta). J Phycol 35:84-88 https://doi.org/10.1046/j.1529-8817.1999.3510084.x
  25. Liu J, Zhu JK (1997) Proline accumulation and salt-stress induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591-596 https://doi.org/10.1104/pp.114.2.591
  26. Min K, Chen K, Arora R (2014) Effect of short-term versus prolonged freezing on freeze-thaw injury and post-thaw recovery in spinach: importance in laboratory freeze-thaw protocols. Environ Exp Bot 106:124-131 https://doi.org/10.1016/j.envexpbot.2014.01.009
  27. Nadeau P, Delaney S, Chouinard L (1987) Effects of cold hardening on the regulation of polyamine levels in wheat (Triticum aestivum L.) and alfalfa (Medicago sativa L.). Plant Physiol 84:73-77 https://doi.org/10.1104/pp.84.1.73
  28. Nakashima K, Satoh R, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1998) A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. Plant Physiol 118:1233-1241 https://doi.org/10.1104/pp.118.4.1233
  29. Robinson SA, Stewart GR, Philips R (1992) Regulation of glutamate dehydrogenase activity in relation to carbon limitation and protein catabolism in carrot cell suspension culture. Plant Physiol 98:1190-1195 https://doi.org/10.1104/pp.98.3.1190
  30. Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263-271 https://doi.org/10.1104/pp.117.1.263
  31. Savoure A, Hua XJ, Bertauche N, van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Mol Gen Genet 254:104-109 https://doi.org/10.1007/s004380050397
  32. Shi H, Ye T, Chen F, Cheng Z, Wang Y, Yang P, Zhang Y, Chan Z (2013) Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation. J Exp Bot 64:1367-1379 https://doi.org/10.1093/jxb/ers400
  33. Shin H, Min K, Arora R (2018) Exogenous salicylic acid improves freezing tolerance of spinach (Spinacia oleraceae L.) leaves. Cryobiology 81:192-200 https://doi.org/10.1016/j.cryobiol.2017.10.006
  34. Shin H, Oh S, Arora R, Kim D (2016) Proline accumulation in response to high temperature in winter-acclimated shoots of Prunus persica: a response associated with growth resumption or heat stress? Can J Plant Sci 96:630-638
  35. Szabados Z, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89-97
  36. Thomashow MF (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
  37. White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90-105 https://doi.org/10.1007/BF00379790
  38. Wisniewski ME, Webb R, Balsamo R, Close TJ, Yu XM, 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
  39. Yang CW, Lin CC, Kao CH (2000) Proline, ornithine, arginine and glutamic acid contents in detached rice leaves. Biol Plant 43:305-307 https://doi.org/10.1023/A:1002733117506
  40. Zhang X, Wang K, Ervin EH, Waltz C, 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