Molecular cloning and differential expression of sHSP gene family members from the resurrection plant Boea hygrometrica in response to abiotic stresses

Biologia (Poland)

Volumn 68, Issue 4, 2013, Pages 651-661

  Zhang, Zhennan ^a,b   Wang, Bo ^b   Sun, Dongmei ^a   Deng, Xin ^b  

^a HEILONGJIANG BAYI AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF BOTANY   (China)

Author keywords

Boea hygrometrica; desiccation tolerance; gene expression; resurrection plant; sHSP

Indexed keywords

BOEA HYGROMETRICA; SELAGINELLA PILIFERA;

EID: 84878962348     PISSN: 00063088     EISSN: 13369563     Source Type: Journal    
DOI: 10.2478/s11756-013-0204-4     Document Type: Article

References (46)

1. Alamillo J., Almoguera C., Bartels D. & Jordano J. 1995. Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol. Biol. 29: 1093-1099.
2. Altschul S. F., Gish W., Miller W., Myers E. W. & Lipman D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Bartels D. 2005. Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr. Comp. Biol. 45: 696-701.
4. Basha E., Friedrich K. L. & Vierling E. 2006. The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J. Biol. Chem. 281: 39943-39952.
5. Bondino H. G., Valle E. M. & Ten Have A. 2012. Evolution and functional diversification of the small heat shock protein/α-crystallin family in higher plants. Planta 235: 1299-1313.
6. Cho E. K. & Hong C. B. 2006. Over-expression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep. 25: 349-358.
7. Chong-Pérez B., Kosky R. G., Reyes M., Rojas L., Oca'na B., Tejeda M., Pérez B. & Angenon G. 2012. Heat shock induced excision of selectable marker genes in transgenic banana by the Cre-lox site-specific recombination system. J. Biotechnol. 159: 265-273.
8. Cosson P., Schurdi-Levraud V., Le Q. H., Sicard O., Caballero M., Roux F., Le Gall O., Candresse T. & Revers F. 2012. The RTM resistance to potyviruses in Arabidopsis thaliana: natural variation of the RTM genes and evidence for the implication of additional genes. PloS. One 7: e39169.
9. Deng X., Hu Z. A., Wang H. X., Wen X. G. & Kuang T. Y. 2003. A comparison of photosynthetic apparatus of the detached leaves of the resurrection plant Boea hygrometrica with its non-tolerant relative Chirita heterotrichia in response to dehydration and rehydration. Plant Science 165: 851-861.
10. Dinakar C., Djilianov D. & Bartels D. 2012. Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci. 182: 29-41.
11. Feder M. E. & Hofmann G. E. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61: 243-282.
12. Garrido C., Paul C., Seigneuric R. & Kampinga H. H. 2012. The small heat shock proteins family: the long forgotten chaperones. Int. J. Biochem. Cell. Biol. 44: 1588-1592.
13. Hamilton E. W. & Heckathorn S. A. 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.
14. Heikkila J. J., Papp J. E., Schultz G. A. & Bewley J. D. 1984. Induction of heat shock protein messenger RNA in maize mesocotyls by water stress, abscisic acid, and wounding. Plant Physiol. 76: 270-274.
15. Helm K. W. & Vierling E. 1989. An Arabidopsis thaliana cDNA clone encoding a low molecular weight heat shock protein. Nucleic Acids Res. 17: 7995.
16. Hu X., Liu R., Li Y., Wang W., Tai F., Xue R. & Li C. 2009. Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul. 60: 225-235.
17. Jaya N., Garcia V. & Vierling E. 2009. Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc. Natl. Acad. Sci. USA 106: 15604-15609.
18. Jiang G., Wang Z., Shang H., Yang W., Hu Z., Phillips J. & Deng X. 2007. Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225: 1405-1420.
19. Kotak S., Vierling E., Bäumlein H. & von Koskull-Döring P. 2007. A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19: 182-195.
20. Lambert W., Koeck P. J., Ahrman E., Purhonen P., Cheng K., Elmlund D., Hebert H. & Emanuelsson C. 2011. Subunit arrangement in the dodecameric chloroplast small heat shock protein Hsp21. Protein Sci. 20: 291-301.
21. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A., Lopez R., Thompson J. D., Gibson T. J. & Higgins D. G. 2007. Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
22. Lee G. J. & Vierling E. 2000. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122: 189-198.
23. Livak K. J. & Schmittgen T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔ C(T)). Method 25: 402-408.
24. Löw D., Brändle K., Nover L. & Forreiter C. 2000. Cytosolic heatstress proteins Hsp17. 7 class I and Hsp17. 3 class II of tomato act as molecular chaperones in vivo. Planta 211: 575-582.
25. Lubaretz O. & Zur Nieden U. 2002. Accumulation of plant small heat-stress proteins in storage organs. Planta 215: 220-228.
26. McDonald E. T., Bortolu M., Koteiche H. A. & McHaourab H. S. 2012. Sequence, structure, and dynamic determinants of Hsp27 (HspB1) equilibrium dissociation are encoded by the N-terminal domain. Biochemistry 51: 1257-1268.
27. Mogk A., Deuerling E., Vorderwülbecke S., Vierling E. & Bukau B. 2003. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50: 585-95.
28. Mymrikov E. V., Seit-Nebi A. S. & Gusev N. B. 2011. Large potentials of small heat shock proteins. Physiol. Rev. 91: 1123-1159.
29. Sato Y. & Yokoya S. 2008. Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17. 7. Plant Cell Rep. 27: 329-334.
30. Seo J. S., Lee Y. M., Park H. G. & Lee J. S. 2006. The intertidal copepod Tigriopus japonicus small heat shock protein 20 gene (Hsp20) enhances thermotolerance of transformed Escherichia coli. Biochem. Biophys. Res. Commun. 340: 901-908.
31. Siddique M., Gernhard S., von Koskull-Doring P., Vierling E. & Scharf K. D. 2008. The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 13: 183-197.
32. Sun L., Liu Y., Kong X., Zhang D., Pan J., Zhou Y., Wang L., Li D. & Yang X. 2012. ZmHSP16. 9, a cytosolic class I small heat shock protein in maize (Zea mays), confers heat tolerance in transgenic tobacco. Plant Cell Rep. 31: 1473-1484.
33. Sun W., van Montagu M. & Verbruggen N. 2002. Small heat shock proteins and stress tolerance in plants. Biochim. Biophys. Acta 1577: 1-9.
34. Tamura K., Dudley J., Nei M. & Kumar S. 2007. MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol. Biol. Evol. 24: 1596-1599.
35. van Aken O., Zhang B., Carrie C., Uggalla V., Paynter E., Giraud E. & Whelan J. 2009. Defining the mitochondrial stress response in Arabidopsis thaliana. Mol. Plant 2: 1310-1324.
36. van Montfort R. L. M., Basha E., Friedrich K. L., Slingsby C. & Vierling E. 2001. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol. 8: 1025-1030.
37. Wang L., Shang H., Liu Y., Zheng M., Wu R., Phillips J., Bartels D. & Deng X. 2009a. A role for a cell wall localized glycinerich protein in dehydration and rehydration of the resurrection plant Boea hygrometrica. Plant Biol. 6: 837-848.
38. 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.
39. Wang Z., Zhu Y., Wang L., Liu X., Liu Y., Phillips J. & Deng X. 2009b. A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230: 1155-1166.
40. Waters E. R. 2013. The evolution, function, structure, and expression of the plant sHSPs. J. Exp. Bot. 64: 391-403.
41. Waters E. R., Aevermann B. D. & Sanders-Reed Z. 2008. Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13: 127-142.
42. Waters E. R. & Riofiorido I. 2007. Evolutionary analysis of the small heat shock proteins in five complete algal genomes. J. Mol. Evol. 65: 162-174.
43. Wehmeyer N. & Vierling E. 2000. The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol. 122: 1099-1108.
44. Whitham S. A., Anderberg R. J., Chisholm S. T. & Carrington J. C. 2000. Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12: 569-582.
45. Ye S. F., Yu S. W., Shu L. B., Wu J. H., Wu A. Z. & Luo L. J. 2012. Expression profile analysis of 9 heat shock protein genes throughout the life cycle and under abiotic stress in rice. Mol. Biol. 4: 336-343.
46. Zhang T., Fang Y., Wang X., Deng X., Zhang X., Hu S. & Yu J. 2012. The complete chloroplast and mitochondrial genome sequences of Boea hygrometrica: insights into the evolution of plant organellar genomes. PloS. One. 7: e30531.