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The protective mechanisms of CaHSP26 in transgenic tobacco to alleviate photoinhibition of PSII during chilling stress

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Abstract

A known sweet pepper cDNA clone, CaHSP26 encoding the chloroplast-localized small heat shock protein (CPsHSP), was isolated and introduced into tobacco plants. It has been reported that CaHSP26 is a member of the CPsHSP gene family related to extreme temperature tolerance in plants. In the present work, the transcripts were detected in the transgenic tobacco lines. The actual quantum yield of photosynthesis (ΦPSII), non-photochemical quenching, and stomatal conductance (gs) in the transgenic lines overexpressing CaHSP26 were higher than those in the wild-type plants under a range of photosynthetic photon flux density during chilling stress. Electron microscopic analysis showed that the transgenic line (L1) had larger size of stomata to lessen stomatal limitation. The activities of ascorbate peroxidase (APX), peroxidase (POD) and catalase (CAT) were also higher in the transgenic lines than those in wild-type plants. Additionally, a significant increase in cis-unsaturated fatty acid contents was observed in transgenic lines due to lower temperatures. These results suggested that CaHSP26 protein plays an important role in protection of PSII by maintaining the antioxidative enzyme activities to avoid or mitigate photooxidation and increasing the fluidity of the thylakoid membrane during chilling stress under low irradiance.

Key message CaHSP26 protein protects PSII by maintaining the antioxidative enzyme activities to avoid or mitigate photooxidation and increases the fluidity of the thylakoid membrane during chilling stress under low irradiance.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  PubMed  CAS  Google Scholar 

  • Al-Whaibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ (Sci) 23:139–150

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering-dependent oxidative stress: effect on anti-oxidant content in Triticum aestivum L. leaves. J Exp Bot 50:375–383

    Article  CAS  Google Scholar 

  • Basha E, Jones C, Wysocki V, Vierling E (2010) Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J Biol Chem 285:11489–11497

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Delong EF, Yayanos AA (1985) Adaptation of the membrane lipids of a deep-sea bacterium to changes in hydrostatic pressure. Science 228:1101–1102

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Vanacker H, Gom′ ez LG, Harbinson J et al (2002) Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review. Plant Physiol Biochem 40:659–668

    Article  CAS  Google Scholar 

  • Gao JP, Chao DY, Lin HX (2008) Toward understanding molecular mechanisms of abiotic stress responses in rice. Rice 1:36–51

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Harrison EP, Willingham NM, Lloyd JC, Raines CA (1998) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204:27–36

    Article  CAS  Google Scholar 

  • Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE, Chen S, Saibil HR, Bucher J (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18:6744–6751

    Article  PubMed  CAS  Google Scholar 

  • Hincha DK (2008) Effects of α-tocopherol (vitamin E) on the stability and lipid dynamics of model membranes mimicking the lipid composition of plant chloroplast membranes. FEBS Lett 582:687–3692

    Article  Google Scholar 

  • Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1997) Antioxidant enzyme and compound responses to chilling stress and their combining abilities in differentially sensitive maize hybrids. Crop Sci 34:857–883

    Article  Google Scholar 

  • Jahnke LS, Hull MR, Long SP (1991) Chilling stress and oxygen metabolizing enzymes in Zea mays and Zea diploperennis. Plant Cell Environ 14:97–104

    Article  CAS  Google Scholar 

  • Jiang C, Xu J, Zhang H, Zhang X, Shi J, Li M, Ming F (2009) A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant Cell Environ 32:1046–1059

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Xu ZY, Na YJ, Yoo YJ, Lee J, Sohn EJ, Hwang I (2011) Small heat shock protein Hsp17.8 functions as an AKR2A cofactor in the targeting of chloroplast outer membrane proteins in Arabidopsis. Plant Physiol 157:132–146

    Article  PubMed  CAS  Google Scholar 

  • Kingston-Smith AH, Harbinson J, Williams J, Foyer CH (1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiol 114:1039–1046

    PubMed  CAS  Google Scholar 

  • Lawlor DW (2002) Limitation to photosynthesis in water-stress leaves: stomata vs metabolism and the role of ATP. Ann Bot 89:871–885

    Article  PubMed  CAS  Google Scholar 

  • Lester EG, Hodges MD, Meyer DR, Munro DK (2004) Pre-extraction preparation (fresh, frozen, freeze-dried, or acetone powdered) and long-term storage of fruit and vegetable tissues: effects on antioxidant enzyme activity. J Agric Food Chem 52:2167–2173

    Article  PubMed  CAS  Google Scholar 

  • Li XG, Meng QW, Jiang GQ, Zou Q (2003) The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water–water cycle. Photosynthetica 41:259–265

    Article  CAS  Google Scholar 

  • Lynch DV, Thompson GA (1982) Low temperature-induced alterations in the chloroplast and microsomal membranes of Dunaliella salina. Plant Physiol 69:1369–1375

    Article  PubMed  CAS  Google Scholar 

  • Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466

    Article  CAS  Google Scholar 

  • Ma QQ, Wang W, Li YH, Li DQ, Zou Q (2006) Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. J Plant Physiol 163:165–175

    Article  PubMed  CAS  Google Scholar 

  • Meer GV, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124

    Article  PubMed  Google Scholar 

  • Mu CJ, Wang SB, Zhang SJ, Pan JJ, Chen N, Li XF, Wang ZY, Liu H (2011) Small heat shock protein LimHSP16.45 protects pollen mother cells and tapetal cells against extreme temperatures during late zygotene to pachytene stages of meiotic prophase I in David Lily. Plant Cell Rep 30:1981–1989

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    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

    Article  PubMed  CAS  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol 47:541–568

    Article  CAS  Google Scholar 

  • Prasad KVSK, Pardha SP (2004) Enhance tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into chloroplasts. Plant Sci 166:1197–1212

    Article  CAS  Google Scholar 

  • Qi Y, Wang H, Zou Y, Liu C, Liu Y, Wang Y, Zhang W (2011) Overexpression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Lett 585:231–239

    Article  PubMed  CAS  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci 166:141–149

    Article  CAS  Google Scholar 

  • Sabehat A, Weiss D, Lurie S (1996) The correlation between heat shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiol 110:531–537

    Article  PubMed  CAS  Google Scholar 

  • Saidi Y, Peter P, Finka A, Cicekli C, Vígh L, Goloubinoff P (2010) Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response. Plant Signal Behav 5:1530–1533. doi:10.4161/psb.5.12.13163

    Google Scholar 

  • Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 190:556–565

    Article  PubMed  CAS  Google Scholar 

  • Sawa K, Teigo A, Yoshinori F, Shiro K (2008) Anti-herbivore structures of Paulownia tomentosa: morphology, distribution, chemical constituents and changes during shoot and leaf development. Ann Bot 101:1035–1047

    Article  Google Scholar 

  • Scebba F, Sebastiani L, Vitagliano C (2001) Activities of antioxidant enzymes during senescence of Prunus armeniaca leaves. Bio. Plant 44:41–46

    Article  CAS  Google Scholar 

  • Soto A, Allona I, Collada C, Guevara MA, Casado R, Cerezo ER, Aragoncillo C, Gomez L (1999) Heterologous expression of a plant small heat shock protein enhances Escherichia coli viability under heat and cold stress. Plant Physiol 120:521–528

    Article  PubMed  CAS  Google Scholar 

  • Sun LP, Liu Y, Kong XP, Zhang D, Pan JW, Zhou Y, Wang L, Li DQ, Yang XH (2012) ZmHSP16.9, a cytosolic class I small heat shock protein in maize (Zea mays), confers heat tolerance in transgenic tobacco. Plant Cell Rep. doi:10.1007/s00299-012-1262-8

  • Suzuki I, Los DA, Murata N (2000) Perception and transduction of low temperature signals to induce desaturation of fatty acids. Biochem Soc Trans 28:628–630

    Article  PubMed  CAS  Google Scholar 

  • 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 224:300–314

    Article  PubMed  CAS  Google Scholar 

  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411

    Article  PubMed  CAS  Google Scholar 

  • Tripp J, Mishra SK, Scharf KD (2009) Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts. Plant Cell Environ 32:123–133

    Article  PubMed  CAS  Google Scholar 

  • Tsien HC, Dreyfus BL, Schmidt EL (1983) Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J Bacteriol 156:888–897

    PubMed  CAS  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wang SY, Faust M (1990) Seasonal changes of membrane lipids in apple shoots. J Am Soc Hort Sci 115:462–467

    CAS  Google Scholar 

  • Wang SY, Lin HS (2006) Effect of plant growth temperature on membrane lipids in strawberry (Fragaria ananassa Duch.). Sci Hortic 108:35–42

    Article  CAS  Google Scholar 

  • Wang SY, Sun T, Whitaker BD, Faust M (1988) Effect of paclobutrazol on membrane lipids in apple seedlings. Physiol Plant 73:560–564

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  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

    Article  CAS  Google Scholar 

  • Williams JP, Khan MU, Mitchell K (1983) Galactolipid biosynthesis in leaves of 16:3- and 18:3-plants. In: Thomson WW, Mudd JB, Gibbs M (eds) Biosynthesis and function of plant lipids. American Society of Plant Physiology Symposium in Botany Riverside, California, pp 28–39

  • Yang XH, Liang Z, Wen XG, Lu CM (2008) Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 66:73–86

    Article  PubMed  CAS  Google Scholar 

  • Yang JS, Wang R, Meng JJ, Bi YP, Xu PL, Guo F, Wan SB, He QW, Li XG (2010) Overexpression of Arabidopsis CBF1 gene in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J Plant Physiol 167:534–539

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura K, Miyao K, Gaber A, Takeda T, Kanaboshi H, Miyasaka H et al (2004) Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J 37:21–33

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Liu CF, Chen XB (2011) Proteomics of rice in response to heat stress and advances in genetic engineering for heat tolerance in rice. Plant Cell Rep 30:2155–2165

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Natural Science Foundation of China (30671242).

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Correspondence to Shangjing Guo.

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Communicated by P. Lakshmanan.

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Li, M., Ji, L., Yang, X. et al. The protective mechanisms of CaHSP26 in transgenic tobacco to alleviate photoinhibition of PSII during chilling stress. Plant Cell Rep 31, 1969–1979 (2012). https://doi.org/10.1007/s00299-012-1309-x

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  • DOI: https://doi.org/10.1007/s00299-012-1309-x

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