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

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Abstract

Plants are sessile organisms that have to cope with different environmental stresses during their life cycle. Photosystem II is one of the most labile processes affected by abiotic stress. The chloroplast small heat shock proteins (Cp-sHSPs) are known to protect photosystem II and thylakoid membranes during heat stress. Previously, we reported several cis-regulatory elements in the promoter regions of Cp-sHSPs of Chenopodium album (Shakeel et al., Plant Physiol Biochem 49:898–908, 2011) and differential regulation of a novel Cp-sHSP family member, CaHSP26.13p, under heat and metal stress (Haq et al., Plant Cell Reports 31:1943–1957, 2012). To further explore the role of Cp-sHSPs in plant stress tolerance, we subjected C. album plants to salt, drought, or cold stress and characterized the accumulation of Cp-sHSP transcripts. Full-length Cp-sHSP transcripts were analyzed for the presence of characteristic domains of Cp-sHSPs and compared with previously known Cp-sHSP homologs and orthologs. Analysis showed that the CaHSP26.13p transcript is differentially regulated under heat, metal, cold, drought, or salt stress. Immunoblot analysis revealed the presence of the precursor proteins (∼26 kDa) synthesized from this transcript. The expression level varied depending on the conditions. Generally, transcript and protein levels were not correlated. This study demonstrates that a single C. album Cp-sHSP had multiple roles under a variety of environmental stresses.

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References

  • 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

    PubMed  CAS  Google Scholar 

  • Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    PubMed  CAS  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    PubMed  CAS  Google Scholar 

  • Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58:79–110

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48:73–84

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    PubMed  CAS  Google Scholar 

  • Cho EK, Hong CB (2006) Overexpression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep 25:349–358

    PubMed  CAS  Google Scholar 

  • Cseke LJ, Tsai CJ, Rogers A, Nelsen MP, White HL, Karnosky DF, Podila GK (2009) Transcriptomic comparison in the leaves of two aspen genotypes having similar carbon assimilation rates but different partitioning patterns under elevated [CO2]. New Phytol 182:891–911

    PubMed  CAS  Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3:117–124

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Dietz KJ, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Ferullo JM, Nespoulous L, Triantaphylides C (1994) Gamma-ray-induced changes in the synthesis of tomato pericarp protein. Plant Cell Environ 17:901–911

    CAS  Google Scholar 

  • Flowers T, Yeo A (1995) Breeding for salinity resistance in crop plants: where next? Aust J Plant Physiol 22:875–884

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    PubMed  CAS  Google Scholar 

  • Franca MB, Panek AD, Eleutherio EC (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A Mol Integr Physiol 146:621–631

    PubMed  CAS  Google Scholar 

  • Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    PubMed  CAS  Google Scholar 

  • Geissler N, Hussin S, Koyro HW (2009) Interactive effects of NaCl salinity and elevated atmospheric CO2 concentration on growth, photosynthesis, water relations and chemical composition of the potential cash crop halophyte Aster tripolium L. Environ Exp Bot 65:220–231

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    CAS  Google Scholar 

  • Hong SW, Lee U, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132:757–767

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61:310–318

    PubMed  CAS  Google Scholar 

  • Khan NA (2003) NaCl inhibited chlorophyll synthesis and associated changes in ethylene evolution and antioxidative enzyme activities in wheat. Biol Plant 47:437–440

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Knight CA, Ackerly DD (2001) Correlated evolution of chloroplast heat shock protein expression in closely related plant species. Am J Bot 88:411–418

    PubMed  CAS  Google Scholar 

  • Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Li P, Ainsworth EA, Leakey AD, Ulanov A, Lozovaya V, Ort DR, Bohnert HJ (2008) Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated [CO2]. Plant Cell Environ 31:1673–1687

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Shulaev V, Cortes D, Miller G, Mittler R (2008) Metabolomics for plant stress response. Physiol Plant 132:199–208

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486

    CAS  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    PubMed  CAS  Google Scholar 

  • Theocharis A, Clement C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    CAS  Google Scholar 

  • Vierling E, Mishkind ML, Schmidt GW, Key JL (1986) Specific heat shock proteins are transported into chloroplasts. Proc Natl Acad Sci 83:361–365

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Wang D, Barua D, Joshi P, LaCroix J, Hamilton EW, Heckathorn SA (2008) Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in 11 (C3, C4, and CAM) species. Am J Bot 95:1–13

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Zhang J, Stewart JMD (2000) Economical and rapid method for extracting cotton genomic DNA. The Journal of Cotton Science 4:193–201

    CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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Acknowledgments

This research was fully supported by the Higher Education Commission of Pakistan grant no. 1212 to SNS. We thank Dr. Eric Schaller for giving us opportunity to complete some of the critical experiments in his lab at Dartmouth College, NH, USA.

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  1. Department of Biochemistry, Faculty of Biological Sciences, Quaid-i-Azam University, 45320, Islamabad, Pakistan

    Noor Ul Haq, Muhammad Ammar & Samina N. Shakeel

  2. Department of Plant Sciences, Quaid-i-Azam University, 45320, Islamabad, Pakistan

    Asghari Bano

  3. Department of Crop and Soil Sciences, College of Agricultural Sciences, Pennsylvania State University, University Park, PA, USA

    Dawn S. Luthe

  4. Department of Environmental Sciences, University of Toledo, Toledo, OH, USA

    Scott A. Heckathorn

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  1. Noor Ul Haq
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Correspondence to Samina N. Shakeel.

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Haq, N.U., Ammar, M., Bano, A. et al. Molecular Characterization of Chenopodium album Chloroplast Small Heat Shock Protein and Its Expression in Response to Different Abiotic Stresses. Plant Mol Biol Rep 31, 1230–1241 (2013). https://doi.org/10.1007/s11105-013-0588-x

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