Simultaneous over-expression of PaSOD and RaAPX in transgenic Arabidopsis thaliana confers cold stress tolerance through increase in vascular lignifications

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Shafi, Amrina ^a,b   Dogra, Vivek ^a   Gill, Tejpal ^a,c   Ahuja, Paramvir Singh ^a,b   Sreenivasulu, Yelam ^a,b  

^a CSIR INSTITUTE OF HIMALAYAN BIORESOURCE TECHNOLOGY   (India)

^b ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBATE PEROXIDASE; CARBOHYDRATE; CHLOROPHYLL; COPPER ZINC SUPEROXIDE DISMUTASE; LIGNIN; PROLINE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

AMINO ACID COMPOSITION; ANTIOXIDANT ACTIVITY; ARABIDOPSIS THALIANA; ARTICLE; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; CHLOROPHYLL CONTENT; COLD TOLERANCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ECOLOGICAL NICHE; ENZYME ACTIVITY; GENE OVEREXPRESSION; LIGNIFICATION; MOLECULAR CLONING; NONHUMAN; PASOD GENE; PLANT GENE; PLANT GROWTH; PLANT STRESS; PLANT YIELD; POLYMERASE CHAIN REACTION; POTENTILLA; POTENTILLA ASTRISANGUINEA; QUANTITATIVE STUDY; RAAPX GENE; RHEUM; RHEUM AUSTRA; SCANNING ELECTRON MICROSCOPY; TRANSGENIC PLANT; UPREGULATION; WILD TYPE; ACCLIMATIZATION; ANALYSIS OF VARIANCE; ARABIDOPSIS; COLD; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

ARABIDOPSIS THALIANA;

ACCLIMATIZATION; ANALYSIS OF VARIANCE; ARABIDOPSIS; ASCORBATE PEROXIDASES; BIOSYNTHETIC PATHWAYS; CHLOROPHYLL; CLONING, MOLECULAR; COLD TEMPERATURE; LIGNIN; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; PLANTS, GENETICALLY MODIFIED; POTENTILLA; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; RHEUM; SUPEROXIDE DISMUTASE;

EID: 84908136032     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110302     Document Type: Article

References (60)

1. Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian J. Med. Biol. Res. 38: 995-1014.
2. Hu D, Klann E, Theils E (2007) Superoxide dismutase and hippocampal function: age and isozymes matter. Antioxidant Redox. Signal. 9: 201-210.
3. Noctor G, Foyer CH (1998). Ascorbate and Glutathione: keeping active oxygen under control. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49: 249-279.
4. Raven EL (2000) Peroxidase-catalyzed oxidation of ascorbate. Structural, spectroscopic and mechanistic correlations in ascorbate peroxidase. Subcell. Biochem. 35: 317-349.
5. Scebba F, Sebastiani L, Vitagliano C (1999) Protective enzymes against activated oxygen species in wheat (Triticum aestivum L.) seedlings: Responses to cold acclimation. J. Plant Physiol. 155: 762-768.
6. Sahoo R, Kumar S, Ahuja PS (2001) Induction of a new isozyme superoxide dismutase at low temperature in Potentilla astrisanguinea Lodd. variety argyrophylla (Wall.ex. Lehm) Griers. J. Plant Physiol.158: 1093-1097.
7. Yogavel M, Mishra PC, Gill J, Bhardwaj PK, Dutt S, et al. (2008) Structure of a superoxide dismutase and implications for copper-ion chelation. Acta Cryst. Biol. Cryst. D64: 892-901.
8. Kumar A, Dutt S, Bagler G, Ahuja PS, Kumar S (2012) Engineering a thermostable superoxide dismutase functional at sub-zero to >50°C, which also tolerates autoclaving. Sci. Rep. 2: 387: 1-8.
9. Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci. 167: 671-677.
10. Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, et al. (2004) Overexpression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stresses and water deficit. Plant Physiol. 121: 231-238.
11. Gill T, Kumar S, Ahuja PS, Sreenivasulu Y (2010b) Over-expression of Potentilla superoxide dismutase improves salt stress tolerance during germination and growth in Arabidopsis thaliana. J. Plant Genet. Transgen. 1: 1-10.
12. Gill T, Dogra V, Kumar S, Ahuja PS, Sreenivasulu Y (2012) Protein dynamics during seed germination under copper stress in Arabidopsis over-expressing Potentilla superoxide dismutase. J. Plant Res. 125: 165-172.
13. Pal AK, Acharya K, Vats SK, Kumar S, Ahuja PS (2013) Over-expression of PaSOD in transgenic potato enhances photosynthetic performance under drought. Biol. Planta. 57: 359-364.
14. Gill T, Sreenivasulu Y, Kumar S, Ahuja PS (2010a) Over-expression of superoxide dismutase exhibits lignifications of vascular structures in Arabidopsis thaliana. J. Plant Physiol. 167: 757-760.
15. Bechtold N, Ellis J, Pelletier GC (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis plants. C. R. Acad. Sci. Paris. 316: 1194-1199.
16. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 473-476.
17. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132: 365-386.
18. reg cells. J. Exp. Med. 208: 1367-1376.
19. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST@) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30: e36.
20. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22: 867-880.
21. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein dye binding. Analytical Biochem. 72: 248-254.
22. Beyer WF, Fridovich I (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 161: 559-566.
23. Lutts S, Kinet J, Bouharmont J (1996). NaCl induced senescence in leaves of rice (Oryza sativa) cultivars differing in salinity resistance. Annal. Bot. 78: 389-398.
24. Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol. Plant. 84: 55-60.
25. Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil. 39: 205-207.
26. Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenoxidase in Beta vulgaris . Plant Physiol. 24: 1-15.
27. Jensen WA (1962) Botanical Histochemistry. p. 408. W. H. Freeman and Co., S. F. and London.
28. Koster KL, Lynch DV (1992) Solute accumulation and compartmentation during the cold acclimation of puma rye. Plant Physiol. 98: 108-113.
29. McKown R, Kuroki G, Warren G (1996) Cold responses of Arabidopsis mutants impaired in freezing tolerance. J. Exp. Bot. 47: 1919-1925.
30. Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120: 391-399.
31. Gajewska E, Sklodowska M, Slaba M, Mazur J (2006) Effect of nickel on antioxidant enzyme activities, praline and chlorophyll contents in wheat shoots. Biol. Plant. 50: 653-659.
32. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 59: 651-681.
33. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14: 1675-1690.
34. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci. 6: 666-671.
35. Xiong L, Shumaker KS, Zhu JK (2002) Cell signaling during cold, drought and salt stresses. Plant Cell 14: 165-183.
36. Fridovich I (1975) Superoxide Dismutase. Ann. Rev. Biochem. 44: 147-159.
37. Dogra V, Ahuja PS, Sreenivasulu Y (2013) Change in protein content during seed germination of a high altitude plant Podophyllum hexandrum Royle. J. Proteom. 78: 26-38.
38. Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in Maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6: 65-74.
39. Sato Y, Murakami T, Funatsuki H, Matsuba S, Saruyama H, et al. (2001) Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings. J. Exp. Bot. 52: 145-151.
40. O'Kane D, Gill V, Boyd P, Burdon R (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198: 371-377.
41. Sowinski P, Rudzinska-Langwald A, Adamczyk J, Kubica I, Fronk J (2005) Recovery of maize seedling growth, development and photosynthetic efficiency after initial growth at low temperature. J. Plant Physiol. 162: 67-80.
42. Rymen B, Fiorani F, Kartal F, Vandepoele K, Inze D, et al. (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol. 143: 1429-1438.
43. Bagnall D, Wolfe JOE, King RW (1983) Chill-induced wilting and hydraulic recovery in mung bean plants. Plant Cell Environ. 6: 457-464.
44. Yoshida R, Kanno A, Kameya T (1996) Cool temperature-induced chlorosis in rice plants (II. Effects of cool temperature on the expression of plastid-encoded genes during shoot growth in darkness). Plant Physiol. 112: 585-590.
45. Nayyar H, Chander K, Kumar S, Bains T (2005a) Glycine betaine mitigates cold stress damage in Chickpea. Agro. Sustain. Deve. 25: 381-388.
46. Kaur G, Kumar S, Nayyar H, Upadhyaya HD (2008) Cold stress injury during the pod- filling phase in chickpea (Cicer arietinum L.): effects on quantitative and qualitative components of seeds. J. Agro. Crop Sci. 194: 457-464.
47. Ohnishi S, Miyoshi T, Shirai S (2010) Low temperature stress at different flower developmental stages affects pollen development, pollination, and pod set in soybean. Environ. Exp. Bot. 69: 56-62.
48. Kumar S, Malik J, Thakur P, Kaistha S, Sharma KD, et al. (2011) Growth and metabolic responses of contrasting chickpea (Cicer arietinum L.) genotypes to chilling stress at reproductive phase. Acta Physiol. Plant. 33: 779-787.
49. Suzuki K, Nagasuga K, Okada M (2008). The chilling injury induced by high root temperature in the leaves of rice seedlings. Plant Cell Physiol. 49: 433-442.
50. Lee HS, Ahsan N, Lee KW, Kim DH, Lee DG, et al. (2007) Simultaneous overexpression of both Cu-Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J. Plant Physiol. 164: 1626-1638.
51. Lu YY, Deng XP, Kwak SS (2010) Over expression of CuZn superoxide dismutase (CuZn SOD) and ascorbate peroxidase (APX) in transgenic sweet potato enhances tolerance and recovery from drought stress. African J. Biotech. 9: 8378-8391.
52. Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, et al. (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J. Exp. Bot. 62: 2599-2613.
53. Yuanyuan M, Yali Z, Jiang L, Hongbo S (2009) Roles of plant soluble sugars and their responses to plant cold stress. African J. Biotech. 8: 2004-2010.
54. Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, et al. (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and Ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant, Cell Environ. 25: 873-882.
55. Barriere Y, Riboulet C, Mechin V, Pichon M, Cardinal AJ, et al. (2007) Genetics and genomics of lignification in grass cell walls based on maize as a model system. G3-Genes Genome Genet. 1: 133-156.
56. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53: 1237-1247.
57. Huang C, Li J, Ke Q, Leonard SS, Jiang BH, et al. (2002) Ultraviolet-induced phosphorylation of p70(S6 K) at Thr(389) and Thr(421)/Ser(424) involves hydrogen peroxide and mammalian target of rapamycin but not Akt and atypical protein kinase C. Cancer Res. 62: 689-697.
58. Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc. Nat. Acad. Sci. USA 99: 4097-4102.
59. Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, et al. (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156: 1364-1374.
60. Moura JCMS, Bonine CAV, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J. Integrat. Plant Biol. 52: 360-376.