The ultrastructure of chilling stress

Plant, Cell and Environment

Volumn 23, Issue 4, 2000, Pages 337-350

  Kratsch, H A ^a   Wise, Robert R ^a  

^a UNIVERSITY OF WISCONSIN OSHKOSH   (United States)

Author keywords

Chilling stress; Chloroplast ultrastructure; Photosynthesis; Programmed cell death; Stress response

Indexed keywords

EID: 0033997197     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-3040.2000.00560.x     Document Type: Review

References (90)

1. Allen J.F. (1992) Protein phosphorylation in the regulation of photosynthesis. Biochimica et Biophysica Acta 1098, 275-335.
2. Ashton F.M., Gifford Jr E.M. & Bisalputra T. (1963) Structural changes in Phaseolus vulgaris induced by atrazine. II. Effects on fine structure of chloroplasts. Botanical Gazette 124, 336-343.
3. Bevins M.A., Madhavan S. & Markwell J. (1993) Two sweetclover (Melilotus alba Desr.) mutants temperature sensitive for chlorophyll expression. Plant Physiology 103, 1123-1131.
4. Bleeker A.B. & Patterson S.E. (1997) Last exit: senescence, abscission and meristem arrest in Arabidopsis. Plant Cell 9, 1169-1179.
5. Browse J. & Somerville C. (1991) Glycerolipid synthesis: biochemistry and regulation. Annual Review of Plant Physiology and Plant Molecular Biology 42, 467-506.
6. Bruggemann W., van der Kooij T.A.W. & van Hasselt P.R. (1992) Long-term chilling of young tomato plants under low light and subsequent recovery. II. Chlorophyll fluorescence, carbon metabolism and activity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Planta 186, 179-187.
7. Buchanan-Wollaston V. (1997) The molecular biology of leaf senescence. Journal of Experimental Botany 48, 181-199.
8. Buckner B., Janick-Buckner D. & Gray J. (1998) Cell-death mechanisms in maize. Trends in Plant Science 3, 218-223.
9. Caspar T., Lin T.P., Kakefuda G., Benbow L., Preiss J. & Somerville C. (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiology 95, 1181-1188.
10. D'Silva I., Poirier G.G. & Heath M.C. (1998) Activation of cysteine proteases in cowpea plants during the hypersensitive response. A form of programmed cell death. Experimental Cell Research 245, 389-399.
11. Deiting U, Zrenner R. & Stitt M. (1998) Similar temperature requirement for sugar accumulation and for the induction of new forms of sucrose phosphate synthase amylase in cold-stored potato tubers. Plant, Cell and Environment 21, 127-138.
12. Del Pozo O. & Lam E. (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Current Biology 8, 1129-1132.
13. Faris J.A. (1926) Cold chlorosis of sugar cane. Phytopathology 16, 885-891.
14. Fellows R.J. & Boyer J.S. (1978) Altered ultrastructure of cells of sunflower leaves having low water potentials. Protoplasma 93, 381-395.
15. Gamalei Y.V., van Bel A.J.E., Pakhomova M.V. & Sjutkina V. (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplastic minor-vein configuration. Planta 194, 443-453.
16. Garber M. & Steponkus P.L. (1976) Alterations in chloroplast thylakoids during cold acclimation. Plant Physiology 57, 681-686.
17. Gazeau C.M. (1985) Influence of the temperature and of the duration of a cryoprotective treatment on the cold resistance of wheat seedlings. Ultrastructure of the leaf primordia nucleolus. Canadian Journal of Botany 63, 663-671.
18. Gemel J., Golinowski W. & Kaniuga Z. (1986) Low-temperature induced changes in chloroplast ultrastructure in relation to changes of Hill reaction activity, manganese and free fatty acid levels in chloroplasts of chilling-sensitive and chilling-resistant plants. Acta Physiologiae Plantarum 8, 135-143.
19. Greenberg J.T. (1996) Programmed cell death: a way of life for plants. Proceedings of the National Academy of Sciences U.S.A. 93, 12094-12097.
20. Greening M., Butterfield F. & Harris N. (1982) Chloroplast ultrastructure during senescence and regreening of flax cotyledons. New Phytologist 92, 279-285.
21. Guy C.L. (1990) Cold acclimation and freezing tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 41, 187-223.
22. Harvey B.M.R. & Fraser T.W. (1980) Paraquat tolerance and susceptible perennial ryegrasses: effects of paraquat treatment on carbon dioxide uptake and ultrastructure of photosynthetic cells. Plant, Cell and Environment 3, 107-117.
23. van Hasselt P. (1974) Photo-oxidative damage to the ultrastructure of Cucumis chloroplasts during chilling. Proceedings Konikl Nederl Akademie Van Wetenschappen Amsterdam Series C 77, 50-56.
24. Heldt H.W. & Saur F. (1971) The inner membrane of the chloroplast envelope as a site of specific metabolite transport. Biochimica et Biophysica Acta 243, 83-91.
25. Humbeck K., Melis A. & Krupinska K. (1994) Effects of chilling on chloroplast development in barley primary foliage leaves. Journal of Plant Physiology 143, 744-749.
26. Huner N.P.A. (1985) Morphological, anatomical, and molecular consequences of growth and development at low temperature in Secale cereale L. CV. puma. American Journal of Botany 72, 1290-1306.
27. Huner N.P.A., Elfman B., Krol M. & McIntosh A. (1984) Growth and development at cold-hardening temperatures. Chloroplast ultrastructure, pigment content and composition. Canadian Journal of Botany 62, 53-60.
28. Huner N.P.A., Öquist G., Hurry V.M., Krol M., Falk S. & Griffith M. (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynthesis Research 37, 19-39.
29. Ishikawa H.A. (1996) Ultrastructural features of chilling injury: injured cells and the early events during chilling of suspension-cultured mung bean cells. American Journal of Botany 83, 825-835.
30. Jabs T., Dietrich R. & Dangl J. (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853-1856.
31. Jacobson M.D., Weil M. & Raff M.C. (1997) Programmed cell death in animal development. Cell 88, 347-354.
32. Jagels R. (1970) Photosynthetic apparatus in Selaginella. II. Changes in plastid ultrastructure and pigment content under different light and temperature regimes. Canadian Journal of Botany 48, 1853-1860.
33. Jones A.M. & Dangl J.L. (1996) Logjam at the Styx: programmed cell death in plants. Trends in Plant Science 4, 114-119.
34. von Kampen J., Nielander U. & Wettern M. (1995) Expression of ubiquitin genes in Chlamydomonas reinhardtii: involvement in stress response and cell cycle. Planta 197, 528-534.
35. Karpilova I., Chugunova N., Bil' K. & Chermnykh L. (1980) Ontogenetic changes of chloroplast ultrastructure, photosynthates, and photosynthate outflow from the leaves in cucumber plants under conditions of reduced night temperature. Soviet Plant Physiology 29, 113-120.
36. Kimball S.L. & Salisbury F.B. (1973) Ultrastructural changes of plants exposed to low temperatures. American Journal of Botany 60, 1028-1033.
37. 2 fixation. American Journal of Botany 55, 695-705.
38. Leddet P.C. & Geneves L. (1982) Effects of low temperatures (+6 degrees C and +2 degrees C) on the fine structure of mitochondria and chloroplasts in the Ephedra tissues, cultivated in vitro. Annales Des Sciences Naturelles 13, 27-49.
39. Leheny E.A. & Theg S.M. (1994) Apparent inhibition of chloroplast protein import by cold temperatures is due to energetic considerations not membrane fluidity. Plant Cell 6, 427-437.
40. Levine A., Pennell R.I., Alvarez M.E., Palmer R. & Lamb C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Current Biology 6, 427-437.
41. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
42. Lyons J.M., Graham D. & Raison J.K. (1979) Low Temperature Stress in Crop Plants. The Role of the Membrane. Academic Press, New York.
43. Ma S., Lin C. & Chen Y. (1990) Comparative studies of chilling stress on alterations of chloroplast ultrastructure and protein synthesis in the leaves of chilling-sensitive (mungbean) and -insensitive (pea) seedlings. Botanical Bulletin of the Academia Sinica 31, 263-272.
44. MacRae E.A. & Ferguson I.B. (1985) Changes in catalase activity and hydrogen peroxide concentration in plants in response to low temperature. Physiologia Planta 65, 51-56.
45. Martin B. (1986) Arrhenius plots and the involvement of thermotropic phase transitions of the thylakoid membrane in chilling impairment of photosynthesis in thermophilic higher plants. Plant, Cell and Environment 9, 323-331.
46. Matzinger D.F. & Wernsman E.A. (1973) Extranuclear temperature-sensitive induced lethality in Nicotiana tabacum. Proceedings of the National Academy of Sciences, USA 70, 108-110.
47. Millerd A., Goodchild D.J. & Spencer D. (1969) Studies on a maize mutant sensitive to low temperature. II. Chloroplast structure, development, and physiology. Plant Physiology 44, 567-583.
48. Minorsky P.V. (1985) An heuristic hypothesis of chilling injury in plants: a role for calcium as the primary physiological transducer of injury. Plant, Cell and Environment 8, 75-94.
49. Mitchell D.E. & Madore M.A. (1992) Patterns of assimilate production and translocation in muskmelon (Cucumis melo L.). II. Low temperature effects. Plant Physiology 99, 966-971.
50. Mittler R. & Lam E. (1995a) Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7, 1951-1962.
51. Mittler R., del Pozo O., Meisel L. & Lam E. (1997) Pathogen-induced programmed cell death in plants, a possible defense mechanism. Developmental Genetics 21, 279-289.
52. Mittler R., Simon L. & Lam E. (1997) Ultrastructural changes and fragmentation of nuclear and chloroplast DNA during the hypersensitive response in tobacco. Journal of Cell Science 110, 1333-1344.
53. Morré D.J., Sellden G., Sundqvist C. & Sandelius A.S. (1991) Stromal low temperature compartment derived from the inner membrane of the chloroplast envelope. Plant Physiology 97, 1558-1564.
54. Mosejev V.V. & Romanovskaya O.I. (1988) Electron-microscopic study of osmium ferricyanide staining in meristematic, extending and differentiated mesophyll cells of winter rye seedlings. Annals of Botany 62, 373-376.
55. Murphy C. & Wilson J.M. (1981) Ultrastructural features of chilling-injury in Episcia reptans. Plant, Cell and Environment 4, 261-265.
56. Musser R.L., Thomas S.A., Wise R.R., Peeler T. & Naylor A.W. (1984) Chloroplast ultrastructure, chlorophyll fluorescence, and pigment composition in chilling-stressed soybeans. Plant Physiology 74, 749-754.
57. Nagata S. (1997) Apoptosis by death factor. Cell 88, 355-365.
58. Nessler C.L. & Wernsman E.A. (1980) Ultrastructural observations of extranuclear temperature-sensitive lethality in Nicotiana tabacum L. Botanical Gazette 141, 9-14.
59. Nessler C.L., Long R.C. & Wernsman E.A. (1980) Physiological observations of extranuclear temperature-sensitive lethality in Nicotiana tabacum L. tobacco genotypes. Zeitschrift Fur Pflanzenphysiologie 99, 27-35.
60. Nicholson D.W. & Thornberry N.A. (1997) Caspases: killer proteases. Trends in Biochemical Science 22, 299-305.
61. O'Neil S.D., Priestley D.A. & Chabot B.F. (1981) Temperature and aging effects on leaf membranes of a cold hardy perennial, Fragaria virginiana. Plant Physiology 68, 1409-1415.
62. Pennell R.I. & Lamb C. (1997) Programmed cell death in plants. Plant Cell 9, 1157-1168.
63. Pomeroy M.K. & Andrews C.J. (1978) Metabolic and ultrastructural changes in winter wheat during ice encasement under field conditions. Plant Physiology 61, 806-811.
64. Post A. & Vesk M. (1992) Photosynthesis, pigments, and chloroplast ultrastructure of an Antarctic liverwort from sun-exposed and shaded sites. Canadian Journal of Botany 70, 2259-2264.
65. Ristic Z. & Ashworth E.N. (1993) Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation. Protoplasma 172, 111-123.
66. Sabehat A., Lurie S. & Weiss D. (1998) Expression of small heat-shock proteins at low temperatures. A possible role in protecting against chilling injuries. Plant Physiology 117, 651-658.
67. Sauter J.J. & Kloth S. (1987) Changes in carbohydrates and ultrastructure in xylem ray cells of Populus in response to chilling. Protoplasma 137, 45-55.
68. Sauter J.J. & van Cleve B. (1991) Biochemical, immunochemical, and ultrastructural studies of protein storage in poplar (Populus x canadensis 'robusta') wood. Planta 183, 92-100.
69. Senser M. & Beck E. (1984) Correlation of chloroplast ultrastructure and membrane lipid composition to the different degrees of frost resistance achieved in leaves of spinach, ivy, and spruce. Journal of Plant Physiology 117, 41-55.
70. Shumway L.H. & Weier T.E. (1967) The chloroplast structure of Iojap maize. American Journal of Botany 54, 773-780.
71. Slack C.R., Roughan P.G. & Bassett H.C. (1974) Selective inhibition of mesophyll chloroplast development in some C4-pathway species by low night temperature. Planta 118, 57-73.
72. Snedden W.A. & Fromm H. (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends in Plant Science 3, 299-304.
73. Somerville C. & Browse J. (1991) Plant lipids: metabolism, mutants and membranes. Science 252, 80-87.
74. 4 plant chloroplasts of Portulaca oleracea L. Zeitschrift Fur Pflanzenphysiologie 87, 37-53.
75. Strand A., Hurry V., Gustafsson P. & Gardestrom P. (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant Journal 12, 605-614.
76. Taylor A.O. & Craig A.S. (1971) Plants under climatic stress. II. low temperature, high light effects on chloroplast ultrastructure. Plant Physiology 47, 719-725.
77. Taylor A.O. & Rowley J.A. (1971) Plants under climatic stress. I. Low temperature, high light effects on photosynthesis. Plant Physiology 47, 713-718.
78. Terashima I. & Inoue Y. (1985) Vertical gradients in photosynthetic properties of spinach chloroplasts dependent on intra-leaf light environment. Plant and Cell Physiology 26, 781-785.
79. Wang M., Oppedijk B.J., Caspers M.P.M., Lamers G.E.M., Boot M.J., Geerlings D.N.G., Bakhuizen B., Meijer A.H. & van Duijn B. (1998) Spatial and temporal regulation of DNA fragmentation in the aleurone of germinating barley. Journal of Experimental Botany 49, 1293-1301.
80. Wise R.R. (1995) Chilling-enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light. Photosynthesis Research 45, 79-97.
81. Wise R.R. & Harris J.B. (1984) The three-dimensional structure of the Cyphomandra betacea chloroplast peripheral reticulum. Protoplasma 119, 222-225.
82. Wise R.R. & Naylor A.W. (1987) Chilling-enhanced photooxidation. The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure. Plant Physiology 83, 272-277.
83. Wise R.R., McWilliam J. & Naylor A.W. (1983) A comparative study of low-temperature-induced ultrastructural alterations of three species with differing chilling sensitivities. Plant, Cell and Environment 6, 525-535.
84. Wolfe J. (1978) Chilling injury in plants - the role of membrane lipid fluidity. Plant, Cell and Environment 1, 241-247.
85. Woods C.M., Reid M.S. & Patterson B.D. (1984a) Response to chilling stress in plant cells, I. Changes in cyclosis and cytoplasmic structure. Protoplasma 121, 8-16.
86. Woods C.M., Polito V.S. & Reid M.S. (1984b) Response to chilling stress in plant cells, II. Redistribution of intracellular calcium. Protoplasma 121, 17-24.
87. Wu J., Lightner J., Warwick N. & Browse J. (1997) Low-temperature damage and subsequent recovery of fab1 mutant Arabidopsis exposed to 2°C. Plant Physiology 113, 347-356.
88. Xu H. & Heath M.C. (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10, 585-597.
89. Yen C.-H. & Yang C.-H. (1998) Evidence for programmed cell death during leaf senescence in plants. Plant and Cell Physiology 39, 922-927.
90. Yun J.G., Hayashi T., Yazawa S., Katoh T. & Yasuda Y. (1996) Acute morphological changes of palisade cells of Saintpaulia leaves induced by a rapid temperature drop. Journal of Plant Research 109, 339-342.