Molecular Characterization of Chenopodium album Chloroplast Small Heat Shock Protein and Its Expression in Response to Different Abiotic Stresses

Plant Molecular Biology Reporter

Volumn 31, Issue 6, 2013, Pages 1230-1241

  Haq, Noor Ul ^a   Ammar, Muhammad ^a   Bano, Asghari ^a   Luthe, Dawn S ^b   Heckathorn, Scott A ^c   Shakeel, Samina N ^a  

^a QUAID I AZAM UNIVERSITY   (Pakistan)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TOLEDO   (United States)

Author keywords

Abiotic stress; Chenopodium album; Cp sHSP; Multiple role

Indexed keywords

CHENOPODIUM ALBUM;

EID: 84888006048     PISSN: 07359640     EISSN: 15729818     Source Type: Journal    
DOI: 10.1007/s11105-013-0588-x     Document Type: Article

References (103)

1. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30: 161-175.
2. Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15: 664-674.
3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
4. Aranjuelo I, Molero G, Erice G, Avice JC, Nogues S (2010) Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). J Exp Bot 62: 111-123.
5. Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylides C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13: 519-527.
6. Barkla BJ, Vera-Estrella R, Hernandez-Coronado M, Pantoja O (2009) Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. Plant Cell 21: 4044-4058.
7. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal Biochem 44: 276-287.
8. Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32: 191-222.
9. Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58: 79-110.
10. Chae L, Sudat S, Dudoit S, Zhu T, Luan S (2009) Diverse transcriptional programs associated with environmental stress and hormones in the Arabidopsis receptor-like kinase gene family. Mol Plant 2: 84-107.
11. Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant Cell Environ 35: 1912-1931.
12. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103: 551-560.
13. Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48: 73-84.
14. Chen Q, Vierling E (1991) Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Mol Gen Genet 226: 425-431.
15. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12: 444-451.
16. Cho EK, Hong CB (2006) Overexpression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep 25: 349-358.
17. 2]. New Phytol 182: 891-911.
18. Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3: 117-124.
19. Dat J, Vandenabeele S, Vranova E, van Montagu M, Inze D, van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57: 779-795.
20. Deeba F, Pandey AK, Ranjan S, Mishra A, Singh R, Sharma YK, Shirke PA, Pandey V (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol Biochem 53: 6-18.
21. Dietz KJ, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155: 1477-1485.
22. Ditmarova L, Kurjak D, Palmroth S, Kmet J, Strelcova K (2009) Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiol 30: 205-213.
23. Downs CA, Heckathorn SA (1998) The mitochondrial small heat-shock protein protects NADH: ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. FEBS Lett 430: 246-250.
24. Downs CA, Ryan SL, Heckathorn SA (1999) The chloroplast small heat shock protein: evidence for a general role in protecting photosystem II against oxidative stress and photoinhibition. J Plant Physiol 155: 488-496.
25. Eckey-Kaltenbach H, Kiefer E, Grosskopf E, Ernst D, Sandermann HJ (1997) Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock. Plant Mol Biol 33: 343-350.
26. Engelbrecht BM, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447: 80-82.
27. Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62: 2599-2613.
28. Ferullo JM, Nespoulous L, Triantaphylides C (1994) Gamma-ray-induced changes in the synthesis of tomato pericarp protein. Plant Cell Environ 17: 901-911.
29. Flowers T, Yeo A (1995) Breeding for salinity resistance in crop plants: where next? Aust J Plant Physiol 22: 875-884.
30. Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17: 507-523.
31. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11: 861-905.
32. Franca MB, Panek AD, Eleutherio EC (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A Mol Integr Physiol 146: 621-631.
33. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64: 97-112.
34. 2 concentration on growth, photosynthesis, water relations and chemical composition of the potential cash crop halophyte Aster tripolium L. Environ Exp Bot 65: 220-231.
35. Gorin N, Heidema FT (1976) Peroxidase activity in golden delicious apples as a possible parameter of ripening and senescence. J Agric Food Chem 24: 200-201.
36. Guo SJ, Zhou HY, Zhang XS, Li XG, Meng QW (2007) Overexpression of CaHSP26 in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J Plant Physiol 164: 126-136.
37. Gupta R, Deswal R (2012) Low temperature stress modulated secretome analysis and purification of antifreeze protein from Hippophae rhamnoides, a Himalayan wonder plant. J Proteome Res 11: 2684-2696.
38. Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126: 1266-1274.
39. Haq NU, Raza S, Luthe DS, Heckathorn SA, Shakeel SN (2012) A dual role for the chloroplast small heat shock protein of Chenopodium album including protection from both heat and metal stress. Plant Molecular Biology Reporter. doi: 10. 1007/s11105-11012-10516-11105.
40. Haralampidis K, Milioni D, Rigas S, Hatzopoulos P (2002) Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 129: 1138-1149.
41. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463-499.
42. Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116: 439-444.
43. Heckathorn SA, Mueller JK, LaGuidice S, Zhu B, Barrett T, Blair B, Dong Y (2004) Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. Am J Bot 91: 1312-1318.
44. Heckathorn SA, Ryan SL, Baylis JA, Wang D, Hamilton IEW, Cundiff L, Luthe DS (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct Plant Biol 29: 933-944.
45. Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57: 1332-1334.
46. Hong SW, Lee U, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132: 757-767.
47. Hu L, Li H, Pang H, Fu J (2012) Responses of antioxidant gene, protein and enzymes to salinity stress in two genotypes of perennial ryegrass (Lolium perenne) differing in salt tolerance. J Plant Physiol 169: 146-156.
48. Jeong SW, Choi SM, Lee DS, Ahn SN, Hur Y, Chow WS, Park YI (2002) Differential susceptibility of photosynthesis to light-chilling stress in rice (Oryza sativa l.) depends on the capacity for photochemical dissipation of light. Mol Cells 13: 419-428.
49. Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zheng SJ (2009) Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced responses under iron-limited conditions in tomato. Plant Physiol 150: 272-280.
50. Jorge I, Navarro RM, Lenz C, Ariza D, Jorrin J (2006) Variation in the holm oak leaf proteome at different plant developmental stages, between provenances and in response to drought stress. Proteomics 6: 207-214.
51. Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61: 310-318.
52. Khan NA (2003) NaCl inhibited chlorophyll synthesis and associated changes in ethylene evolution and antioxidative enzyme activities in wheat. Biol Plant 47: 437-440.
53. Kim KH, Alam I, Kim YG, Sharmin SA, Lee KW, Lee SH, Lee BH (2012) Overexpression of a chloroplast-localized small heat shock protein OsHSP26 confers enhanced tolerance against oxidative and heat stresses in tall fescue. Biotechnol Lett 34: 371-377.
54. Knight CA, Ackerly DD (2001) Correlated evolution of chloroplast heat shock protein expression in closely related plant species. Am J Bot 88: 411-418.
55. Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16: 681-687.
56. Koca M, Bor M, Ozdemir F, Turkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60: 344-351.
57. Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25: 275-294.
58. Lee BH, Won SH, Lee HS, Miyao M, Chung WI, Kim IJ, Jo J (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245: 283-290.
59. Legnaioli T, Cuevas J, Mas P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28: 3745-3757.
60. 2]. Plant Cell Environ 31: 1673-1687.
61. Li Q, Yu B, Gao Y, Dai AH, Bai JG (2011) Cinnamic acid pretreatment mitigates chilling stress of cucumber leaves through altering antioxidant enzyme activity. J Plant Physiol 168: 927-934.
62. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55: 1151-1191.
63. Liu ZJ, Zhang XL, Bai JG, Suo BX, Xu PL, Wang L (2009) Exogenous paraquat changes antioxidant enzyme activities and lipid peroxidation in drought-stressed cucumber leaves. Sci Hortic 121: 138-143.
64. Lu P, Sang WG, Ma KP (2008) Differential responses of the activities of antioxidant enzymes to thermal stresses between two invasive Eupatorium species in China. J Integr Plant Biol 50: 393-401.
65. Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC, Sohrabi E (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust J Crop Sci 4: 580-585.
66. Matteucci M, D'Angeli S, Errico S, Lamanna R, Perrotta G, Altamura MM (2011) Cold affects the transcription of fatty acid desaturases and oil quality in the fruit of Olea europaea L. genotypes with different cold hardiness. J Exp Bot 62: 3403-3420.
67. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25: 239-250.
68. Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17: 1829-1838.
69. Ning J, Li X, Hicks LM, Xiong L (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152: 876-890.
70. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757: 742-749.
71. Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169: 596-604.
72. Pandey V, Ranjan S, Deeba F, Pandey AK, Singh R, Shirke PA, Pathre UV (2010) Desiccation-induced physiological and biochemical changes in resurrection plant, Selaginella bryopteris. J Plant Physiol 167: 1351-1359.
73. Ramirez V, Coego A, Lopez A, Agorio A, Flors V, Vera P (2009) Drought tolerance in Arabidopsis is controlled by the OCP3 disease resistance regulator. Plant J 58: 578-591.
74. Rhoades J, Loveday J (1990) Salinity in irrigated agriculture. In: Steward BA, Nielsen DR (eds) American Society of Civil Engineers, Irrigation of agricultural crops (Monograph 30). American Society of Agronomists, Madison, pp. 1089-1142.
75. Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69: 225-232.
76. Saravanavel R, Ranganathan R, Anantharaman P (2011) Effect of sodium chloride on photosynthetic pigments and photosynthetic characteristics of Avicennia officinalis seedlings. Recent Research in Science and Technology 3: 177-180.
77. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
78. Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61: 661-671.
79. Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151: 275-289.
80. Shakeel S, Haq NU, Heckathorn SA, Hamilton EW, Luthe DS (2011) Ecotypic variation in chloroplast small heat-shock proteins and related thermotolerance in Chenopodium album. Plant Physiol Biochem 49: 898-908.
81. Shakeel SN, Haq NU, Heckathorn S, Luthe DS (2012) Analysis of gene sequences indicates that quantity not quality of chloroplast small HSPs improves thermotolerance in C4 and CAM plants. Plant Cell Reports 31: 1943-1957.
82. Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Biochem 54: 78-88.
83. Shulaev V, Cortes D, Miller G, Mittler R (2008) Metabolomics for plant stress response. Physiol Plant 132: 199-208.
84. Siddiqi EH, Ashraf M, Al-Qurainy F, Akram NA (2011) Salt-induced modulation in inorganic nutrients, antioxidant enzymes, proline content and seed oil composition in safflower (Carthamus tinctorius L.). J Sci Food Agric 91: 2785-2793.
85. Soares-Cordeiro AS, Driscoll SP, Arrabaca MC, Foyer CH (2010) Dorsoventral variations in dark chilling effects on photosynthesis and stomatal function in Paspalum dilatatum leaves. J Exp Bot 62: 687-699.
86. Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42: 481-486.
87. Sun W, van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577: 1-9.
88. Theocharis A, Clement C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235: 1091-1105.
89. Uemura M, Steponkus PL (1999) Cold acclimation in plants: relationship between the lipid composition and the cryostability of the plasma membrane. J Plant Res 112: 245-254.
90. van Berkel J, Salamini F, Gebhardt C (1994) Transcripts accumulating during cold storage of potato (Solanum tuberosum L.) tubers are sequence related to stress-responsive genes. Plant Physiol 104: 445-452.
91. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579-620.
92. Vierling E, Mishkind ML, Schmidt GW, Key JL (1986) Specific heat shock proteins are transported into chloroplasts. Proc Natl Acad Sci 83: 361-365.
93. Villar-Salvador P, Planelles R, Oliet J, Penuelas-Rubira JL, Jacobs DF, Gonzalez M (2004) Drought tolerance and transplanting performance of holm oak (Quercus ilex) seedlings after drought hardening in the nursery. Tree Physiol 24: 1147-1155.
94. 2 on the tolerance of photosynthesis to acute heat stress in 11 (C3, C4, and CAM) species. Am J Bot 95: 1-13.
95. Wang D, Luthe DS (2003) Heat sensitivity in a bentgrass variant. Failure to accumulate a chloroplast heat shock protein isoform implicated in heat tolerance. Plant Physiol 133: 319-327.
96. Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47: 325-338.
97. Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25: 195-210.
98. Xu PL, Guo YK, Bai JG, Shang L, Wang XJ (2008) Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. Physiol Plant 132: 467-478.
99. Yu JQ, Zhou YH, Huang LF, Allen DJ (2002) Chill-induced inhibition of photosynthesis: genotypic variation within Cucumis sativus. Plant Cell Physiol 43: 1182-1188.
100. Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58: 1068-1082.
101. Zhang J, Stewart JMD (2000) Economical and rapid method for extracting cotton genomic DNA. The Journal of Cotton Science 4: 193-201.
102. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6: 66-71.
103. Zobayed SMA, Afreen F, Kozai T (2005) Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John's wort. Plant Physiol Biochem 43: 977-984.