Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato

Plant Cell, Tissue and Organ Culture

Volumn 117, Issue 1, 2014, Pages 1-16

  Liu, Degao ^a   He, Shaozhen ^a   Zhai, Hong ^a   Wang, Lianjun ^a   Zhao, Yao ^a   Wang, Bing ^a   Li, Ruijie ^a   Liu, Qingchang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

IbP5CR; Proline; ROS scavenging system; Salt tolerance; Sweetpotato

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; CARBOXYLATION; OXYGEN;

IBP5CR; PROLINE; ROS SCAVENGING SYSTEM; SALT TOLERANCE; SWEET POTATO;

GENES;

EID: 84896923597     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-013-0415-y     Document Type: Article

References (85)

1. Adams E, Frank L (1980) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49: 1005-1061.
2. Ahmad I, Hellebust JA (1988) The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae. Plant Physiol 88: 348-354.
3. Alia, Saradhi PP, Mohanty P (1991) Proline enhances primary photochemical activities in isolated thylakoid membranes of Brassica juncea by arresting photo inhibitory damage. Biochem Biophsy Res Commun 181: 1238-1244.
4. Alia, Saradhi PP, Mohanty P (1997) Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. J Photochem Photobiol 38: 253-257.
5. Alia, Mohanty P, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21: 195-200.
6. Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130: 1443-1453.
7. Al-Taweel K, Iwaki T, Yabuta Y, Shigeoka S, Murata N, Wadano A (2007) A bacterial transgene for catalase protects translation of D1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol 145: 258-265.
8. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
9. Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69: 26-36.
10. +-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176: 232-240.
11. Blum A, Ebercon A (1976) Genotypic responses in sorghum to drought stress. III. Free proline accumulation and drought resistance. Crop Sci 16: 428-431.
12. Boggess SF, Aspinall D, Paleg LG (1976a) Stress metabolism. IX. The significance of end-product inhibition of proline biosynthesis and of compartmentation in relation to stress-induced proline accumulation. Aust J Plant Physiol 3: 513-525.
13. Boggess SF, Stewart CR, Aspinall D, Paleg LG (1976b) Effect of water stress on proline synthesis from radioactive precursors. Plant Physiol 58: 398-401.
14. Buhl MB, Stewart CR (1983) Effects of NaCl on proline synthesis and utilization in excised barley leaves. Plant Physiol 72: 664-667.
15. Chen HJ, Su CT, Lin CH, Huang GJ, Lin YH (2010) Expression of sweet potato cysteine protease SPCP2 altered developmental characteristics and stress responses in transgenic Arabidopsis plants. J Plant Physiol 167: 838-847.
16. Chinnusamy V, Zhu JH, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. In: Setlow JK (ed) Genetic engineering. Springer, New York, pp 141-177.
17. 1-pyrroline-5-carboxylate reductase transgenic soybean plants subjected to osmotic and drought stress. Plant Growth Regul 32: 13-26.
18. De Ronde JA, Cress WA, Krüger GHJ, Strasser RJ, van Staden J (2004a) Photosynthetic response of transgenic soybean plants, containing an ArabidopsisP5CR gene, during heat and drought stress. J Plant Physiol 161: 1211-1224.
19. De Ronde JA, Laurie RN, Caetano T, Greyling MM, Kerepesi I (2004b) Comparative study between transgenic and non-transgenic soybean lines proved transgenic lines to be more drought tolerant. Euphytica 138: 123-132.
20. 1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet 221: 299-305.
21. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4: 215-223.
22. Delauney AJ, Hu CAA, Kishor PBK, Verma DPS (1993) Cloning of ornithine δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268: 18673-18678.
23. Dhir SK, Oglesby J, Bhagsari AS (1998) Plant regeneration via embryogenesis and transient gene expression in sweet potato protoplasts. Plant Cell Rep 17: 665-669.
24. Fan WJ, Zhang M, Zhang HX, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS ONE 7: e37344.
25. Fernández-Falcón M, Hernández M, Alvarez CE, Borges AA (2006) Variation in nutrition along time and relative chlorophyll content of Leucospermum cordifolium cv. 'High Gold', and their relationship with chlorotic symptoms. Sci Hortic 107: 373-379.
26. Fricke W, Akhiyarova G, Veselov D, Kudoyarova G (2004) Rapid and tissue-specific changes in ABA and in growth rate in response to salinity in barley leaves. J Exp Bot 55: 1115-1123.
27. Gao S, Yuan L, Zhai H, Liu CL, He SZ, Liu QC (2011) Transgenic sweetpotato plants expressing an LOS5 gene are tolerant to salt stress. Plant Cell Tissue Organ Cult 107: 205-213.
28. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48: 909-930.
29. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21: 79-102.
30. He SZ, Han YF, Wang YP, Zhai H, Liu QC (2009) In vitro selection and identification of sweetpotato (Ipomoea batatas (L.) Lam.) plants tolerant to NaCl. Plant Cell, Tissue Organ Cult 96: 69-74.
31. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347: 1-39.
32. 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci U S A 89: 9354-9358.
33. + accumulation and proline metabolism in potato (Solanum tuberosum). PLoS ONE 8: e60183.
34. Jain S, Kumar D, Jain M, Chaudhary P, Deswal R, Sarin NB (2012) Ectopic overexpression of a salt stress-induced pathogenesis-related class 10 protein (PR10) gene from peanut (Arachis hypogaea L.) affords broad spectrum abiotic stress tolerance in transgenic tobacco. Plant Cell, Tissue Organ Cult 109: 19-31.
35. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
36. Jiang T, Zhai H, Wang FB, Yang NK, Wang B, He SZ, Liu QC (2013) Cloning and characterization of a carbohydrate metabolism-associated gene IbSnRK1 from sweetpotato. Sci Hortic 158: 22-32.
37. Jung Y, Park J, Choi Y, Yang JG, Kim D, Kim BG, Roh K, Lee DH, Auh CK, Lee S (2010) Expression analysis of proline metabolism-related genes from Halophyte Arabis stelleri under osmotic stress conditions. J Integr Plant Biol 52: 891-903.
38. 1-pyrroline-5-carboxylate synthetase increases proline production and confers Osmotolerance in transgenic plants. Plant Physiol 108: 1387-1394.
39. Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8: 1323-1335.
40. Koca H, Ozdemir F, Turkan I (2006) Effect of salt stress on lipid peroxidation and superoxide dismutase and peroxidase activities of Lycopersicon esculentum and L. pennellii. Biol Plant 50: 745-748.
41. Kocsy G, Laurie R, Szalai G, Szilágyi V, Simon-Sarkadi L, Galiba G, De Ronde JA (2005) Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stresses. Physiol Plantarum 124: 227-235.
42. Kumar V, Shriram V, Kavi Kishor PB, Jawali N, Shitole MG (2010) Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over-expressing P5CSF129A gene. Plant Biotechnol Rep 4: 37-48.
43. Liu QC (2011) Sweetpotato omics and biotechnology in China. Plant Omics 4: 295-301.
44. Liu QC, Zhai H, Wang Y, Zhang DP (2001) Efficient plant regeneration from embryogenic suspension cultures of sweetpotato. In Vitro Cell Dev Biol plant 37: 564-567.
45. Ma L, Zhou E, Gao L, Mao X, Zhou R, Jia J (2008) Isolation, expression analysis and chromosomal location of P5CR gene in common wheat (Triticum aestivum L.). S Afr J Bot 74: 705-712.
46. Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31: 699-712.
47. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plantarum 133: 481-489.
48. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33: 453-467.
49. Munns R (2002) The impact of salinity stress. http://www. plantstress. com/Articles/index. asp.
50. Nanjo T, Fujita M, Seki M, Kato T, Tabata S, Shinozaki K (2003) Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant Cell Physiol 44: 541-548.
51. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60: 324-349.
52. Parida AK, Dagaonkar VS, Phalak MS, Aurangabadkar LP (2008) Differential responses of the enzymes involved in proline biosynthesis and degradation in drought tolerant and sensitive cotton genotypes during drought stress and recovery. Acta Physiol Plant 30: 619-627.
53. Peng XJ, Zhang LX, Zhang LX, Liu ZJ, Cheng LQ, Yang Y, Shen SH, Chen SY, Liu GS (2013) The transcriptional factor LcDREB2 cooperates with LcSAMDC2 to contribute to salt tolerance in Leymus chinensis. Plant Cell, Tissue Organ Cult 113: 245-256.
54. Rhodes D, Handa S, Bressan RA (1986) Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol 82: 890-903.
55. Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5: 69-76.
56. Saradhi P, Alia P, Arora S, Prasad KV (1995) Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem Biophys Res Commun 209: 1-5.
57. Savouré 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.
58. T method. Nat Protocols 3: 1101-1108.
59. Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, De Ronde JA (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biol Plantarum 50: 793-796.
60. Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14: 2837-2847.
61. Sivakumar P, Sharmila P, Pardha Saradhi P (2000) Proline alleviates salt-stress-induced enhancement in ribulose-1, 5-bisphosphate oxygenase activity. Biochem Biophs Res Commun 279: 512-515.
62. Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28: 1057-1060.
63. Stewart CR (1981) Proline accumulation: biochemical aspects. In: Paleg LG, Aspinall D (eds) Physiology and biochemistry of drought Resistance in plants. Academic Press, Sydney, pp 243-259.
64. Sun XL, Ji W, Ding XD, Bai X, Cai H, Yang SS, Qian X, Sun MZ, Zhu YM (2013) GsVAMP72, a novel Glycine soja R-SNARE protein, is involved in regulating plant salt tolerance and ABA sensitivity. Plant Cell, Tissue Organ Cult 113: 199-215.
65. 1-pyrroline -5- carboxylate reductase in root/nodule and leaf of soybean. Plant Physiol 99: 1642-1649.
66. Takahashi S, Murata N (2008) How do environmental stresses accelerate photo inhibition? Trends in Plant Sci 13: 178-182.
67. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428: 419-438.
68. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35: 753-759.
69. Verbruggen N, Villarroel R, Montagu MV (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103: 771-781.
70. Walton EF, Clark CJ, Boldingh HL (1991) Effect of hydrogen cyanamide on amino acid profiles in kiwifruit buds during bud break. Plant Physiol 97: 1256-1259.
71. Walton EF, Podivinsky E, Wu RM, Reynolds PHS, Young LW (1998) Regulation of proline biosynthesis in kiwifruit buds with and without hydrogen cyanamide treatment. Physiol Plantarum 102: 171-178.
72. Wang LJ, He SZ, Zhai H, Liu DG, Wang YN, Liu QC (2013) Molecular cloning and functional characterization of a salt tolerance-associated gene IbNFU1 from sweetpotato. J Integr Agric 12: 27-35.
73. Watad AEA, Reinhold L, Lerner HR (1983) Comparison between a stable NaCl-selected Nicotiana cell line and the wild type. Plant Physiol 73: 624-629.
74. 1-pyrrolline-5-carboxylate reductase (proC) gene in Pea (Pisum sativum L.). Plant Physiol 100: 1464-1470.
75. Wu QY, Lin JL, Liu JZ, Wang XF, Lim WS, Oh MM, Park JG, Rajashekar CB, Whitham SA, Cheng NH, Hirschi KD, Park S (2012) Ectopic expression of Arabidopsis glutaredoxin AtGRXS17 enhances thermo tolerance in tomato. Plant Biotechnol J 10: 945-955.
76. Wyn Jones RG, Storeys R (1978) Salt stress and comparative physiology in the Gramineae. Glycine betaine and proline accumulation in two salt and water stressed barley cultivars. Aust J Plant Physiol 5: 817-829.
77. Yang A, Dai XY, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63: 2541-2556.
78. Yang CW, Deng W, Tang N, Wang XM, Yan F, Lin DB, Li ZG (2013a) Overexpression of ZmAFB2, the maize homologue of AFB2 gene, enhances salt tolerance in transgenic tobacco. Plant Cell, Tissue Organ Cult 112: 171-179.
79. Yang L, Han HJ, Liu MM, Zuo ZJ, Zhou KQ, Lü JC, Zhu YR, Bai YL, Wang Y (2013b) Overexpression of the Arabidopsis photo respiratory pathway gene, serine: glyoxylate aminotransferase (AtAGT1), leads to salt stress tolerance in transgenic duckweed (Lemna minor). Plant Cell, Tissue Organ Cult 113: 407-416.
80. Yang YL, Yang F, Li XN, Shi RX, Lu J (2013c) Signal regulation of proline metabolism in callus of the halophyte Nitraria tangutorum Bobr. grown under salinity stress. Plant Cell, Tissue Organ Cult 112: 33-42.
81. + antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell, Tissue Organ Cult 111: 49-57.
82. Yu B, Zhai H, Wang YP, Zang N, He SZ, Liu QC (2007) Efficient Agrobacterium tumefaciens-mediated transformation using embryogenic suspension cultures in sweetpotato Ipomoea batatas (L.) Lam. Plant Cell, Tissue Organ Cult 90: 265-273.
83. Zang N, Zhai H, Gao S, Chen W, He SZ, Liu QC (2009) Efficient production of transgenic plants using the bar gene for herbicide resistance in sweetpotato. Sci Hortic 122: 649-653.
84. Zhang H, Han B, Wang T, Chen SX, Li HY, Zhang YH, Dai SJ (2012a) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11: 49-67.
85. + antiporter gene, DmNHX1, confers salt tolerance when expressed transiently in Nicotiana benthamiana or stably in Arabidopsis thaliana. Plant Cell, Tissue Organ Cult 110: 189-200.