Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance

Plant Physiology

Volumn 138, Issue 2, 2005, Pages 882-897

  Larkindale, Jane ^a   Hall, Jennifer D ^b   Knight, Marc R ^c   Vierling, Elizabeth ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GENES; GROWTH KINETICS; METABOLISM; MUTAGENESIS;

ACTIVE OXYGEN SPECIES; PROTEIN INDUCTION; SALICYLIC ACID PATHWAYS;

PLANTS (BOTANY);

ENZYMES; GENES; GENETIC ENGINEERING; GROWTH; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

HEAT SHOCK PROTEIN;

ACCLIMATIZATION; ARABIDOPSIS; ARTICLE; GENETICS; HEAT; LIGHT; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ACCLIMATIZATION; ARABIDOPSIS; HEAT; HEAT-SHOCK PROTEINS; LIGHT; MUTATION; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; SEEDLING; SIGNAL TRANSDUCTION;

EID: 26944443125     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.062257     Document Type: Review

References (61)

1. Alfonso M, Yruela I, Almarcegui S, Torrado E, Perez MA, Picorel R (2001) Unusual tolerance to high temperatures in a new herbicide-resistant D1 mutant from Glycine max (L.) Merr. cell cultures deficient in fatty acid desaturation. Planta 212: 573-582
2. Argandona VH, Chaman M, Cardemil L, Munoz O, Zuniga GE, Corcuera LJ (2001) Ethylene production and peroxidase activity in aphid-infested barley. J Chem Ecol 27: 53-68
3. Bariola PA, MacIntosh GC, Green PJ (1999) Regulation of S-like ribonuclease levels in Arabidopsis. Antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation. Plant Physiol 119: 331-342
4. Berardini TZ, Bollman K, Sun H, Poethig RS (2001) Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291: 2405-2407
5. Bortier K, Dekelver G, De Temmerman L, Ceulemans R (2001) Stem injection of Populus nigra with EDU to study ozone effects under field conditions. Environ Pollut 111: 199-208
6. Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32: 191-222
7. Burke JJ, O'Mahoney PJ, Oliver MJ (2000) Isolation of Arabidopsis mutants lacking components of acquired thermotolerance. Plant Physiol 123: 575-588
8. Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38: 432-447
9. Dat JF, Foyer CH, Scott IM (1998a) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118: 1455-1461
10. 2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116: 1351-1357
11. Drané P, Compe E, Catez P, Chymkowitch P, Egly J-M (2004) Selective regulation of vitamin D receptor-responsive genes by TFIIH. Mol Cell 16: 187-197
12. Dubaele S, Proietti De Santis L, Bienstock RJ, Keriel A, Stefanini M, Van Houten B, Egly JM (2003) Basal transcription defect discriminates between xeroderma pigmentosum and trichothiodystrophy in XPD patients. Mol Cell 11: 1635-1646
13. Flahaut S, Benachour A, Giard JC, Boutibonnes P, Auffray Y (1996) Defense against lethal treatments and de novo protein synthesis induced by NaCl in Enterococcus faecalis ATCC 19433. Arch Microbiol 165: 317-324
14. Friant S, Meier KD, Riezman H (2003) Increased ubiquitin-dependent degradation can replace the essential requirement for heat shock protein induction. EMBO J 22: 3783-3791
15. Ghosh S, Gepstein SS, Heikkila JJ, Dumbroff EB (1988) Use of a scanning densitometer of an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissues. Anal Biochem 169: 227-233
16. Gong M, Li YJ, Chen SZ (1998) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153: 488-496
17. Hall AE (2001) Crop Responses to the Environment. CRC Press, Boca Raton, FL
18. Haughn GW, Somerville C (1986) Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol Gen Genet 204: 430-434
19. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 125: 189-198
20. Hong SW, Lee U, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132: 757-767
21. Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97: 4392-4397
22. Hong SW, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27: 25-35
23. Horváth I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F, Vigh L (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a "fluidity gene". Proc Natl Acad Sci USA 95: 3513-3518
24. Hugly S, Kunst L, Somerville C (1991) Linkage relationships of mutations that affect fatty-acid composition in Arabidopsis. J Hered 82: 484-488
25. James DW, Dooner HK (1991) Novel seed lipid phenotypes in combinations of mutants altered in fatty-acid biosynthesis in Arabidopsis. Theor Appl Genet 82: 409-412
26. Jenkins ME, Suzuki TC, Mount DW (1997) Evidence that heat and ultraviolet radiation activate a common stress-response program in plants that is altered in the uvh6 mutant of Arabidopsis thaliana. Plant Physiol 115: 1351-1358
27. Kampinga HH, Brunsting JF, Stege GJ, Burgman PW, Konings AW (1995) Thermal protein denaturation and protein aggregation in cells made thermotolerant by various chemicals: role of heat shock proteins. Exp Cell Res 219: 536-546
28. Kato M, Hayakawa Y, Hyodo H, Ikoma Y, Yano M (2000) Wound-induced ethylene synthesis and expression and formation of 1-aminocyclopropane-1- carboxylate (ACC) synthase, ACC oxidase, phenylalanine ammonia-lyase, and peroxidase in wounded mesocarp tissue of Cucurbita maxima. Plant Cell Physiol 41: 440-447
29. Kapoor M, Sreenivasan GM, Goel N, Lewis J (1990) Development of thermotolerance in Neurospora crassa by heat shock and other stresses eliciting peroxidase induction. J Bacteriol 172: 2798-2801
30. Klueva NY, Maestri E, Marmiroli N, Nguyen HT (2001) Mechanisms of thermotolerance in crops. In AS Basra ed, Crop Responses and Adaptations to Temperature Stress. Food Products Press, Binghamton, NY, pp 177-217
31. Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161: 405-413
32. Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128: 682-695
33. Larkindale J, Mishkind M, Vierling E (2005) Plant responses to high temperature. In MA Jenks, PM Hasegawa, eds, Plant Abiotic Stress. Blackwell Scientific Publications, Oxford (in press)
34. Liu Z, Hong S-W, Escobar M, Vierling E, Mitchell DL, Mount DW, Hall JD (2003) Arabidopsis UVH6, a homolog of human XPD and yeast RAD3 DNA repair genes functions in DNA repair and is essential for plant growth. Plant Physiol 132: 1405-1414
35. Ludwig-Muller J, Krishna P, Forreiter C (2000) A glucosinolate mutant of Arabidopsis is thermosensitive and defective in cytosolic Hsp90 expression after heat stress. Plant Physiol 123: 949-958
36. Manning WJ, Flagler RB, Frenkel MA (2003) Assessing plant response to ambient ozone: growth of ozone-sensitive loblolly pine seedlings treated with ethylenediurea or sodium erythorbate. Environ Pollut 126: 73-81
37. Massie MR, Lapoczka EM, Boggs KD, Stine KE, White GE (2003) Exposure to the metabolic inhibitor sodium azide induces stress protein expression and thermotolerance in the nematode Caenorhabditis elegans. Cell Stress Chaperones 8: 1-7
38. Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjarvi J (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol 130: 1918-1926
39. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287: 476-479
40. Nie X, Singh RP, Tai GC (2002) Molecular characterization and expression analysis of 1-aminocyclopropane-1-carboxylate oxidase homologs from potato under abiotic and biotic stresses. Genome 45: 905-913
41. Nieto-Sotelo J, Kannan KB, Martinez LM, Segal C (1999) Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene 230: 187-195
42. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359
43. Riezman H (2004) Why do cells require heat shock proteins to survive heat stress? Cell Cycle 3: 61-63
44. Ristic Z, Cass DD (1992) Chloroplast structure after water and high temperature stress in 2 lines of maize that differ in endogenous levels of abscisic acid. Int J Plant Sci 153: 186-196
45. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696
46. Robertson AJ, Ishikawa M, Gusta LV, MacKenzie SL (1994) Abscisic acid-induced heat tolerance in Bromus inermis Leyss cell-suspension cultures. Heat-stable, abscisic acid-responsive polypeptides in combination with sucrose confer enhanced thermostability. Plant Physiol 105: 181-190
47. Rojas A, Almoguera C, Jordano J (1999) Transcriptional activation of a heat shock gene promoter in sunflower embryos: synergism between ABI3 and heat shock factors. Plant J 20: 601-610
48. Sandermann H (2000) Active oxygen species as mediators of plant immunity: three case studies. Biol Chem 381: 649-653
49. Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31: 629-638
50. Svejstrup JQ, Vichi P, Egly JM (1996) The multiple roles of transcription/repair factor TFIIH. Trends Biochem Sci 9: 346-350
51. Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30: 431-446
52. Thatcher LF, Anderson JP, Singh KB (2005) Plant defense responses: What have we learnt from Arabidopsis? Funct Plant Biol 32: 1-19
53. Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91(phox) homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517-522
54. Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J 14: 365-370
55. Vacca RA, de Pinto MC, Valenti D, Passarella S, Marra E, De Gara L (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco bright-yellow 2 cells. Plant Physiol 134: 1100-1112
56. Van Breusegem F, Vranova E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161: 405-414
57. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579-620
58. Wehmeyer N, Hernandez LD, Finkelstein RR, Vierling E (1996) Synthesis of small heat-shock proteins is part of the developmental program of late seed maturation. Plant Physiol 112: 747-757
59. 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
60. Yan N, Doelling JH, Falbel TG, Durski AM, Vierstra RD (2000) The ubiquitin-specific protease family from Arabidopsis. AtUBP1 and 2 are required for the resistance to the amino acid analog canavanine. Plant Physiol 124: 1828-1843
61. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247-273