Heat shock-induced biphasic Ca2+ signature and OsCaM1-1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.)

Plant, Cell and Environment

Volumn 35, Issue 9, 2012, Pages 1543-1557

  Wu, Hui Chen ^a   Luo, Dan Li ^a   Vignols, Florence ^b   Jinn, Tsung Luo ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Apoplastic Ca2+; Ca2+ signalling; Calmodulin; Heat shock protein; Heat shock signalling

Indexed keywords

CALCIMYCIN; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHLORIDE; CALMODULIN; MESSENGER RNA; VEGETABLE PROTEIN;

ADAPTATION; CALCIUM; GENE EXPRESSION; HEAT SHOCK; HERB; INHIBITOR; ION; PHYSIOLOGICAL RESPONSE; PROTEIN; RICE; SIGNALING; TEMPERATURE TOLERANCE; TRANSGENIC PLANT;

ADAPTATION; ARABIDOPSIS; ARTICLE; CALCIUM SIGNALING; CELL NUCLEUS; CYTOLOGY; CYTOSOL; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGY; PLANT CELL; PLANT GENE; PLANT ROOT; PROTEIN TRANSPORT; RICE; TEMPERATURE; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; CALCIMYCIN; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHLORIDE; CALCIUM SIGNALING; CALMODULIN; CELL NUCLEUS; CYTOSOL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HEAT-SHOCK RESPONSE; ORYZA SATIVA; PLANT CELLS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; RNA, MESSENGER; TEMPERATURE;

ARABIDOPSIS; ORYZA SATIVA;

EID: 84864835501     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2012.02508.x     Document Type: Article

References (71)

1. Baniwal S.K., Bharti K., Chan K.Y., etal. (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences 29, 471-487.
2. Boonburapong B. & Buaboocha T. (2007) Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins. BMC Plant Biology 7, 4.
3. Bouche N., Yellin A., Snedden W.A. & Fromm H. (2005) Plant-specific calmodulin-binding proteins. Annual Review of Plant Biology 56, 435-466.
4. Busch W., Wunderlich M. & Schöffl F. (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. The Plant Journal 41, 1-14.
5. Carrington J.C. & Freed D.D. (1990) Cap-independent enhancement of translation by a plant potyvirus 5′ nontranslated region. Journal of Virology 64, 1590-1597.
6. Charng Y.Y., Liu H.C., Liu N.Y., Hsu F.C. & Ko S.S. (2006) Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiology 140, 1297-1305.
7. Charng Y.Y., Liu H.C., Liu N.Y., Chi W.T., Wang C.N., Chang S.H. & Wang T.T. (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiology 143, 251-262.
8. Clayton H., Knight M.R., Knight H., McAinsh M.R. & Hetherington A.M. (1999) Dissection of the ozone-induced calcium signature. The Plant Journal 17, 575-579.
9. Clough S.J. & Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
10. Cooper P. & Meddings J.B. (1991) Erythrocyte membrane fluidity in malignant hyperthermia. Biochimica et Biophysica Acta 1069, 151-156.
11. Craske H., Takeo T., Gerasimenko O., Vaillant C., Torok K., Petersen O.H. & Tepikin A.V. (1999) Hormone-induced secretory and nuclear translocation of calmodulin: oscillations of calmodulin concentration with the nucleus as an integrator. Proceedings of the National Academy of Sciences of the United States of America 96, 4426-4431.
12. Friedberg F. & Taliaferro L. (2005) Calmodulin genes in zebrafish (revisited). Molecular Biology Reports 32, 55-60.
13. Gong M., van der Luit A.H., Knight M.R. & Trewavas A.J. (1998) Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiology 116, 429-437.
14. Guan J.C., Jinn T.L., Yeh C.H., Feng S.P., Chen Y.M. & Lin C.Y. (2004) Characterization of the genomic structures and selective expression profiles of nine class I small heat shock protein genes clustered on two chromosomes in rice (Oryza sativa L.). Plant Molecular Biology 56, 795-809.
15. Hong S.W. & Vierling E. (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. The Plant Journal 27, 25-35.
16. Horváth I., Glatz A., Varvasovszki V., etal. (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a 'fluidity gene. Proceedings of the National Academy of Sciences of the United States of America 95, 3513-3518.
17. Hsu S.F. & Jinn T.L. (2010) AtHSBP functions in seed development and the motif is required for subcellular localization and interaction with AtHSFs. Plant Signaling & Behavior 5, 1042-1044.
18. Hsu S.F., Lai H.C. & Jinn T.L. (2010) Cytosol-localized heat shock factor-binding protein, AtHSBP, functions as a negative regulator of heat shock response by translocation to the nucleus and is required for seed development in Arabidopsis. Plant Physiology 153, 773-784.
19. Ikeda M., Mitsuda N. & Ohme-Takagi M. (2011) Arabidopsis HsfB1 and HsfB2b act as repressors for the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiology 157, 1243-1254.
20. Jinn T.L., Wu S.H., Yeh C.H., Hsieh M.H., Yeh Y.C., Chen Y.M. & Lin C.Y. (1993) Immunological kinship of class I low molecular weight heat shock proteins and thermostabilization of soluble proteins in vitro among plants. Plant and Cell Physiology 34, 1055-1062.
21. Jinn T.L., Chang P.F.L., Chen Y.M., Key J.L. & Lin C.Y. (1997) Tissue-type-specific heat-shock response and immunolocalization of class I low-molecular-weight heat-shock proteins in soybean. Plant Physiology 114, 429-438.
22. Kaplan B., Davydov O., Knight H., Galon Y., Knight M.R., Fluhr R. & Fromm H. (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. The Plant Cell 18, 2733-2748.
23. Kim M.C., Chung W.S., Yun D.J. & Cho M.J. (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Molecular Plant 2, 13-21.
24. Kotak S., Larkindale J., Lee U., von Koskull-Doring P., Vierling E. & Scharf K.D. (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310-316.
25. Krishna P. & Kanelakis K.C. (2003) The 70-kDa protein bound to hsp90 in wheat germ lysate is a plant homologue of animal Hop. Physiologia Plantarum 119, 456-462.
26. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
27. Larkindale J. & Knight M.R. (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128, 682-695.
28. Lecourieux D., Mazars C., Pauly N., Ranjeva R. & Pugin A. (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. The Plant Cell 14, 2627-2641.
29. Lee Y.L., Chang P.F.L., Yeh K.W., Jinn T.L., Kung C.C.S., Lin W.C., Chen Y.M. & Lin C.Y. (1995) Cloning and characterization of a cDNA encoding an 18.0-kDa class-I low-molecular-weight heat-shock protein from rice. Gene 165, 223-227.
30. Lehel C., Los D., Wada H., Gyorgyei J., Horvath I., Kovacs E., Murata N. & Vigh L. (1993) A second groEL-like gene, organized in a groESL operon is present in the genome of Synechocystis sp. PCC 6803. Journal of Biological Chemistry 268, 1799-1804.
31. Li B., Liu H.T., Sun D.Y. & Zhou R.G. (2004) Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant and Cell Physiology 45, 627-634.
32. Lin C.Y., Roberts J.K. & Key J.L. (1984) Acquisition of thermotolerance in soybean seedlings: synthesis and accumulation of heat-shock proteins and their cellular localization. Plant Physiology 74, 152-160.
33. Lindquist S. & Craig E.A. (1988) The heat-shock proteins. Annual Review of Genetics 22, 631-677.
34. Liu H.T., Li B., Shang Z.L., Li X.Z., Mu R.L., Sun D.Y. & Zhou R.G. (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiology 132, 1186-1195.
35. Liu H.T., Sun D.Y. & Zhou R.G. (2005) Ca2+ and AtCaM3 are involved in the expression of heat shock protein gene in Arabidopsis. Plant Cell & Environment 28, 1276-1284.
36. Liu H.T., Li G.L., Chang H., Sun D.Y., Zhou R.G. & Li B. (2007) Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant Cell & Environment 30, 156-164.
37. Liu H.T., Gao F., Li G.L., Han J.L., Liu D.L., Sun D.Y. & Zhou R.G. (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. The Plant Journal 55, 760-773.
38. Lohmann C., Eggers-Schumacher G., Wunderlich M. & Schoffl F. (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Molecular Genetics and Genomics 271, 11-21.
39. Luan S., Kudla J., Rodriguez-Concepcion M., Yalovsky S. & Gruissem W. (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. The Plant Cell 14, S389-S400.
40. van der Luit A.H., Olivari C., Haley A., Knight M.R. & Trewavas A.J. (1999) Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiology 121, 705-714.
41. Ma L.G., Xu X.D., Cui S.J. & Sun D.Y. (1999) The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. The Plant Cell 11, 1351-1363.
42. McAinsh M.R. & Pittman J.K. (2009) Shaping the calcium signature. New Phytologist 181, 275-294.
43. Mishra S.K., Tripp J., Winkelhaus S., Tschiersch B., Theres K., Nover L. & Scharf K.D. (2002) In the complex family of heat stress transcription factors, HSfA1 has a unique role as master regulator of thermotolerance in tomato. Genes & Development 16, 1555-1567.
44. Mosser D.D., Kotzbauer P.T., Sarge K.D. & Morimoto R.I. (1990) In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proceedings of the National Academy of Sciences of the United States of America 87, 3748-3752.
45. Nishizawa A., Yabuta Y., Yoshida E., Maruta T., Yoshimura K. & Shigeoka S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. The Plant Journal 48, 535-547.
46. Nover L., Bharti K., Doring P., Mishra S.K., Ganguli A. & Scharf K.D. (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress & Chaperones 6, 177-189.
47. Poutrain P., Mazars C., Thiersault M., Rideau M. & Pichon O. (2009) Two distinct intracellular Ca2+-release components act in opposite ways in the regulation of the auxin-dependent MIA biosynthesis in Catharanthus roseus cells. Journal of Experimental Botany 60, 1387-1398.
48. Queitsch C., Hong S.W., Vierling E. & Lindquist S. (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant Cell 12, 479-492.
49. Raynal P., Kuijpers G., Rojas E. & Pollard H.B. (1996) A rise in nuclear calcium translocates annexins IV and V to the nuclear envelope. FEBS Letters 392, 263-268.
50. Rentel M.C. & Knight M.R. (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiology 135, 1471-1479.
51. Rudd J.J. & Franklin-Tong V.E. (2001) Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytologist 151, 7-33.
52. Saidi Y., Finka A., Muriset M., Bromberg Z., Weiss Y.G., Maathuis F.J.M. & Goloubinoff P. (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. The Plant Cell 21, 2829-2843.
53. Saidi Y., Finka A. & Goloubinoff P. (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytologist 190, 556-565.
54. Sarkar N.K., Kim Y.K. & Grover A. (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10, 393.
55. Schmid M., Davison T.S., Henz S.R., Pape U.J., Demar M., Vingron M., Scholkopf B., Weigel D. & Lohmann J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nature Genetics 37, 501-506.
56. Schöffl F., Prändl R. & Reindl A. (1998) Regulation of the heat-shock response. Plant Physiology 117, 1135-1141.
57. Shou H.X., Bordallo P., Fan J.B., Yeakley J.M., Bibikova M., Sheen J. & Wang K. (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proceedings of the National Academy of Sciences of the United States of America 101, 3298-3303.
58. 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.
59. Swindell W.R., Huebner M. & Weber A.P. (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8, 125.
60. Tamaoki T. (1991) Use and specificity of staurosporine, UCN-01, and calphostin C as protein kinase inhibitors. Methods in Enzymology 201, 340-347.
61. Teruel M.N., Chen W., Persechini A. & Meyer T. (2000) Differential codes for free Ca2+-calmodulin signals in nucleus and cytosol. Current Biology 10, 86-94.
62. Thorogate R. & Török K. (2004) Ca2+-dependent and -independent mechanisms of calmodulin nuclear translocation. Journal of Cell Science 117, 5923-5936.
63. Tseng T.S., Tzeng S.S., Yeh K.W., Yeh C.H., Chang F.C., Chen Y.M. & Lin C.Y. (1993) The heat-shock pesponse in rice seedlings: isolation and expression of cDNAs that encode class-I low-molecular-weight heat-shock proteins. Plant and Cell Physiology 34, 165-168.
64. Vierling E. (1991) The roles of heat-shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 42, 579-620.
65. White P.J. (2000) Calcium channels in higher plants. Biochimica et Biophysica Acta 1465, 171-189.
66. Wu H.C. & Jinn T.L. (2010) Heat shock-triggered Ca2+ mobilization accompanied by pectin methylesterase activity and cytosolic Ca2+ oscillation are crucial for plant thermotolerance. Plant Signaling & Behavior 5, 1252-1256.
67. Wu H.C., Hsu S.F., Luo D.L., Chen S.J., Huang W.D., Lur H.S. & Jinn T.L. (2010) Recovery of heat shock-triggered released apoplastic Ca2+ accompanied by pectin methylesterase activity is required for thermotolerance in soybean seedlings. Journal of Experimental Botany 61, 2843-2852.
68. Yang T. & Poovaiah B.W. (2003) Calcium/calmodulin-mediated signal network in plants. Trends in Plant Science 8, 505-512.
69. Yoo S.D., Cho Y.H. & Sheen J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2, 1565-1572.
70. Yoshida T., Sakuma Y., Todaka D., Maruyama K., Qin F., Mizoi J., Kidokoro S., Fujita Y., Shinozaki K. & Yamaguchi-Shinozaki K. (2008) Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochemical and Biophysical Research Communications 368, 515-521.
71. Zhang W., Zhou R.G., Gao Y.J., Zheng S.Z., Xu P., Zhang S.Q. & Sun D.Y. (2009) Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiology 149, 1773-1784.