Cold stress induces biochemical changes, fatty acid profile, antioxidant system and gene expression in Capsella bursa pastoris L.

Acta Physiologiae Plantarum

Volumn 40, Issue 9, 2018, Pages

  Wani, Mubashir Ahmad ^a   Jan, Nelofer ^a   Qazi, Hilal Ahmad ^a   Andrabi, Khurshid Iqbal ^a   John, Riffat ^a  

^a UNIVERSITY OF KASHMIR   (India)

Author keywords

Capsella; Cold stress; Cold tolerance; Membrane damage; qPCR; Reactive oxygen species

Indexed keywords

EID: 85052385969     PISSN: 01375881     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11738-018-2747-z     Document Type: Article

References (77)

1. Akrami M, Arzani A (2018) Physiological alterations due to field salinity stress in melon (Cucumis melo L.). Acta Physiol Plant 40:1–14
2. Baek KH, Skinner DZ (2012) Production of reactive oxygen species by freezing stress and the protective roles of antioxidant enzymes in plants. J Agric Chem Environ 1:34
3. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant soil 39:205–207
4. Bohn M, Luthje S, Sperling P, Heinz E, Dorffling K (2007) Plasma membrane lipid alterations induced by cold acclimation and abscisic acid treatment of winter wheat seedlings differing in frost resistance. J plant Physiol 164:146–156
5. Boudet J, Buitink J, Hoekstra FA, Rogniaux H, Larre C, Satour P, Leprince O (2006) Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140:1418–1436. 10.1104/pp.105.074039
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
7. Cai HM, Dong YY, Li YY, Li DX, Peng CY, Zhang ZZ (2016) Physiological and cellular responses to fluoride stress in tea (Camellia sinensis) leaves. Acta Physiol Plant 38:144–155. 10.1007/s11738-016-2156-0
8. Cyril J, Powell GL, Duncan RR, Baird WV (2002) Changes in membrane polar lipid fatty acids of seashore paspalum in response to low temperature exposure. Crop Sci 42:2031–2037
9. Dey PM (1990) Oligosaccharides. In: Dey PM, Harbome JB (eds) Methods in plant biochemistry, vol 2. Academic Press, San Diego, CA, pp 189–218
10. Ding T, Pang J, Wang Q, Yang N, Gao LP (2012) Effect of exogenous glycine betaine treatment on chilling injury of hot pepper. Guangdong Agric Sci 21:2015
11. Ding X, Zhang H, Wang L, Qian H, Qi X, Xiao J (2015) Effect of barley antifreeze protein on thermal properties and water state of dough during freezing and freeze-thaw cycles. Food Hydrocoll 47:32–40
12. Duxbury AC, Yentsch CS (1956) Plankton pigment nomography. J Air Pollut Control Assoc 16:145–150
13. Ebrahimi M, Abdullah SNA, Aziz MA, Namasivayam P (2016) Oil palm EgCBF3 conferred stress tolerance in transgenic tomato plants through modulation of the ethylene signaling pathway. J Plant Physiol 202:107–120
14. El-Aal HAHMA (2012) Lipid peroxidation end-products as a key of oxidative stress: effect of antioxidant on their production and transfer of free radicals. In Lipid Peroxidation. 10.5772/45944 (InTech)
15. Fan J, Ren J, Zhu W, Amombo E, Fu J, Chen L (2014) Antioxidant responses and gene expression in bermudagrass under cold stress. J Am Soc Hortic Sci 139:699–705
16. Feng W, Indner H, Robbins NE, Dinneny JR (2016) Growing out of stress: the role of cell-and organ-scale growth control in plant water-stress responses. Plant Cell 28:1769–1782
17. Flexas J, Diaz-Espejo A, Gago J, Galle A, Galmes J, Gulias J, Medrano H (2014) Photosynthetic limitations in Mediterranean plants: a review. Environ Exp Bot 103:12–23
18. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883
19. Gao SQ, Chen M, Xia LQ, Xiu HJ, Xu ZS, Li LC, Zhao CP, Cheng XG, Ma YZ (2009) A cotton (Gossypium hirsutum) DREB-binding transcription factor gene, GhDREB, confers enhanced tolerance to drought, high salt, and freezing stresses intransgenic wheat. Plant Cell Rep 28:301–311
20. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307
21. Halliwell B, Foyer CH (1978) Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta 139:9–17
22. Hara M, Terashima S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333–1339
23. Harb A, Awad D, Samarah N (2015) Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare L.) under controlled severe drought. J Plant Interact 10:109–116
24. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466
25. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthrocyanin and other interfering compounds. Planta 207:604–611
26. Holden M (1961) The breakdown of chlorophyll by chlorophyllase. Biochem J 78:359
27. Honjoh KI, Matsumoto H, Shimizu H, Ooyama K, Tanaka K, Oda Y, Iio M (2000) Cryoprotective activities of group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Biosci Biotechnol Biochem 64:1656–1663
28. Hu ZR, Fan JB, Xie Y, Amombo E, Liu A, Gitau MM (2016) Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin. Plant Physiol Biochem 100:94–104. 10.1016/j.plaphy.2016.01.008
29. Huang HR, Liu JJ, Xu Y, Lascoux M, Ge XJ, Wright SI (2018) Homeologue-specific expression divergence in the recentlyformed tetraploid Capsella bursa-pastoris (Brassicaceae). New Phytol. 10.1111/nph.15299
30. Hundertmark M, Hincha D (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118
31. Jan N, Hussain M, Andrabi KI (2009) Cold resistance in plants: a mystery unresolved. Electron J Biotechnol 12:15
32. Jan N, Majeed U, Andrabi KI, John R (2018) Cold stress modulates osmolytes and antioxidant system in Calendula officinalis. Acta Physiol Plant 40:73
33. Janska A, Marsik P, Zelenkova S, Ovesna J (2009) Cold stress and acclimation—what is important for metabolic adjustment. Plant Biol 12:395–405
34. John R, Ganeshan U, Singh BN, Kaul T, Reddy MK, Sopory SK, Rajam MV (2016) Over-expression of topoisomerase II enhances salt stress tolerance in tobacco. Front Plant Sci 7:1280
35. John R, Raja V, Ahmad M, Jan N, Majeed U, Ahmad S, Kaul T (2017) Trehalose: metabolism and role in stress signalling in plants. In stress signaling in plants: genomics and proteomics perspective, vol 2, pp 261–275. Springer International Publishing, Berlin
36. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168
37. Karabudak T, Bor M, Ozdemir F, Turkan I (2014) Glycine betaine protects tomato (Solanum lycopersicum) plants at low temperature by inducing fatty acid desaturase 7 and lipoxygenase gene expression. Mol Biol Rep 41:1401–1410
38. Kawakami S, Matsumoto Y, Matsunaga A, Mayama S, Mizuno M (2002) Molecular cloning of ascorbate peroxidase in potato tubers and its response during storage at low temperature. Plant Sci 163:829–836
39. Knight MR, Heather K (2012) Low temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 4:737–751
40. Koc E, Islek C, Ustun AS (2010) Effect of cold on protein, proline, phenolic compounds and chlorophyll content of two pepper (Capsicum annuum L.) varieties. Gazi Univ J Sci 23:1–6
41. Kovacs Z, Simon-Sarkadi L, Vashegyi I, Kocsy G (2012) Different accumulation of free amino acids during short-and long-term osmotic stress in wheat. Sci World J 1:2012
42. Lee BH, Zhu JK (2010) Phenotypic analysis of Arabidopsis mutants: electrolyte leakage after freezing stress. Cold Spring Harbor Protoc 2010:4970
43. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta DeltaC(T)) method. Methods 25:402–408
44. MacLachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of achlorophyll mutant of barley. Can J Bot 41:1053–1062
45. Maraghni M, Gorai M, Neffati M (2010) Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Ziziphus lotus. S Afr J Bot 76:453–459
46. Martinez V, Nieves-Cordones M, Lopez-Delacalle M, Rodenas R, Mestre TC, Garcia-Sanchez F, Rubio F, Nortes PA, Mittler R, Rivero RM (2018) Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules 23(3):535
47. Moore S, Stein WH (1948) Partition chromatography of amino acids on starch. Ann N Y Acad Sci 49:265–278
48. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
49. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K et al (2000) Organization and expression of two arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
50. Nanculao GD, Herrera ML, Carcamo MP, Velasquez VB (2014) Relative expression of genes related with cold tolerance in temperate rice at the seedling stage. Afr J Biotechnol 13:2506–2512
51. Omolade O, Muller AE, Jung C, Melzer S (2016) BvPRR7 is a cold responsive gene with a clock function in beet. Biol Plant 60:95–104
52. Palonen P, Buszard D, Donnelly D (2000) Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol Plant 110:93–401
53. Patane C, Cavallaro V, Cosentino SL (2009) Germination and radicle growth in unprimed and primed seeds of sweet sorghum as affected by reduced water potential in NaCl at different temperatures. Crops Prod 30:1–8
54. Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69. 10.3389/fpls.2015.00069
55. Rahimi A (2013) Seed priming improves the germination performance of cumin (Cuminum syminum L.) under temperature and water stress. Ind Crops Prod 42:454–460
56. Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157. 10.1016/j.envexpbot.2017.02.010
57. Rinalducci S, Egidi MG, Karimzadeh G, Jazii FR, Zolla L (2011) Proteomic analysis of a spring wheat cultivar in response to prolonged cold stress. Electrophoresis 32:1807–1818
58. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009
59. Sanchez-Ballesta MT, Rodrigo MJ, Lafuente MT, Granell A, Zacarias L (2004) Dehydrin from citrus, which confers in vitro dehydration tolerance and freezing protection activity, is constitutive and highly expressed in the flavedo of fruit but responsive to cold and water stress in leaves. J Agric Food Chem 52:1950–1957. 10.1021/jf035216
60. Shan TM, Sun YJ, Jin P, Xu J, Zheng YH (2014) Effects of glycine betaine on loquat fruit quality during cold storage. IV Int Symp Loquat 1092:131–137
61. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 10.1155/2012/217037
62. Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447. 10.1093/aob/mcu239
63. Sullivan CY, Ross WM (1979) Selecting for drought and heat resistance in grain sorghum. In: Mussell H, Staples RC (eds) Stress physiology in crop plants. Wiley, New York, pp 263–281
64. Tahmasebi A, Pakniyat H (2015) Comparative analysis of some biochemical responses of winter and spring wheat cultivars under low temperature. Int J Agric Agric 7:14–22
65. Teixeira FK, Menezes-Benavente L, Galvao VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300
66. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599
67. Tobeh A, Jamaati-e-Somarin S (2012) Low temperature stress effect on wheat cultivars germination. Afr J Microbiol 6:1265–1269
68. 2 levels and stored at 0°C. Front Plant Sci 8:1591
69. 2+ homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694
70. Wang HS, Yu C, Zhu ZJ, Yu XC (2011) Overexpression in tobacco of a tomato GMPase gene improves tolerance to both low and high temperature stress by enhancing antioxidation capacity. Plant Cell Rep 30:1029–1040
71. Wang Z, Chen L, Yang H, Wang A (2015) Effect of exogenous glycine betaine on qualities of button mushrooms (Agaricus bisporus) during postharvest storage. Eur Food Research Technol 240:41–48
72. Xu S, Jiang Y, Cui W, Jin Q, Zhang Y, Bu D, Fu J, Wang R, Zhou F, Shen W (2017) Hydrogen enhances adaptation of rice seedlings to cold stress via the reestablishment of redox homeostasis mediated by miRNA expression. Plant Soil 414:53–67
73. Yoon YE, Kuppusamy S, Cho KM, Kim PJ, Kwack YB, Lee YB (2017) Influence of cold stress on contents of soluble sugars, vitamin C and free amino acids including gamma-aminobutyric acid (GABA) in spinach (Spinacia oleracea). Food Chem 215:185–192
74. Yuanyuan M, Yali Z, Jiang L, Hongbo S (2009) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Biotechnol 8:10
75. Zeng X, Ling H, Yang J, Li Y, Guo S (2018) LEA proteins from Gastrodia elata enhance tolerance to low temperature stress in Escherichia coli. Gene 646:136–142
76. Zhang H, Jiang Y, He Z, Ma M (2005) Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol 162:977–984
77. Zhang P, Liu S, Chen K (2013) Characterization and expression analysis of a glutathione reductase gene from Antarctic moss Pohlia nutans. Plant Mol Biol Rep 31:1068–1076