Accumulation of small heat-shock protein homologs in the endoplasmic reticulum of cortical parenchyma cells in mulberry in association with seasonal cold acclimation.

Cortical parenchyma cells of mulberry (Morus bombycis Koidz.) trees acquire extremely high freezing tolerance in winter as a result of seasonal cold acclimation. The amount of total proteins in endoplasmic reticulum (ER)-enriched fractions isolated from these cells increased in parallel with the process of cold acclimation. Protein compositions in the ER-enriched fraction also changed seasonally, with a prominent accumulation of 20-kD (WAP20) and 27-kD (WAP27) proteins in winter. The N-terminal amino acid sequence of WAP20 exhibited homology to ER-localized small heat-shock proteins (smHSPs), whereas that of WAP27 did not exhibit homology to any known proteins. Like other smHSPs, WAP20 formed a complex of high molecular mass in native-polyacrylamide gel electrophoresis. Furthermore, not only WAP20 but also 21-kD proteins reacted with antibodies against WAP20. Fractionation of the crude microsomes by isopycnic sucrose-gradient centrifugation revealed that both WAP27 and WAP20 were distributed on a density corresponding to the fractions with higher activity of ER marker enzyme, suggesting localization of these proteins in the ER. When ER-enriched fractions were treated with trypsin in the absence of detergent, WAP20 and WAP27 were undigested, suggesting localization of these proteins inside the ER vesicle. The accumulation of a large quantity of smHSPs in the ER in winter as a result of seasonal cold acclimation indicates that these proteins may play a significant role in the acquisition of freezing tolerance in cortical parenchyma cells of mulberry trees.

[1]  K. Nakahigashi,et al.  Regulation of the heat-shock response. , 1999, Current opinion in microbiology.

[2]  M. Thomashow Role of cold-responsive genes in plant freezing tolerance. , 1998, Plant physiology.

[3]  C. Guy,et al.  Association of Proteins with the Stress 70 Molecular Chaperones at Low Temperature: Evidence for the Existence of Cold Labile Proteins in Spinach☆ , 1998 .

[4]  J. Staden,et al.  Dissecting the roles of osmolyte accumulation during stress , 1998 .

[5]  D. Weiss,et al.  Expression of small heat-shock proteins at low temperatures. A possible role in protecting against chilling injuries. , 1998, Plant physiology.

[6]  C. Guy,et al.  Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. , 1998, Plant physiology.

[7]  S. Yoshida,et al.  Accumulation of 19-kDa plasma membrane polypeptide during induction of freezing tolerance in wheat suspension-cultured cells by abscisic acid. , 1997, Plant & cell physiology.

[8]  A. Lafta,et al.  Cell-Wall Changes and Cell Tension in Response to Cold Acclimation and Exogenous Abscisic Acid in Leaves and Cell Cultures , 1996, Plant physiology.

[9]  T. Close,et al.  Seasonal patterns of dehydrins and 70-kDa heat-shock proteins in bark tissues of eight species of woody plants , 1996 .

[10]  M. Dunn,et al.  The molecular biology of plant acclimation to low temperature , 1996 .

[11]  D. Weiss,et al.  The Correlation between Heat-Shock Protein Accumulation and Persistence and Chilling Tolerance in Tomato Fruit , 1996, Plant physiology.

[12]  M. Griffith,et al.  Chapter 3 Extracellular ice formation in freezing-tolerant plants , 1996 .

[13]  M. Wisniewski,et al.  Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus × canadensis Moench "robusta") wood. , 1996 .

[14]  J. Maindonald,et al.  Reducing External Chilling Injury in Stored 'Hass' Avocados with Dry Heat Treatments , 1995 .

[15]  Graham Collins,et al.  Heat shock proteins and chilling sensitivity of mung bean hypocotyls , 1995 .

[16]  T. Mccollum,et al.  Immersion of cucumber fruit in heated water alters chilling-induced physiological changes , 1995 .

[17]  Garrett J. Lee,et al.  Structure and in Vitro Molecular Chaperone Activity of Cytosolic Small Heat Shock Proteins from Pea(*) , 1995, The Journal of Biological Chemistry.

[18]  S. Hill,et al.  Cold-Induced Accumulation of hsp90 Transcripts in Brassica napus , 1995, Plant physiology.

[19]  E. Heberle‐Bors,et al.  The expression of a small heat shock gene is activated during induction of tobacco pollen embryogenesis by starvation , 1995 .

[20]  E. Vierling,et al.  An Endomembrane-Localized Small Heat-Shock Protein from Arabidopsis thaliana , 1995, Plant physiology.

[21]  C. Guy,et al.  Perspectives of plant cold tolerance: physiology and molecular responses. , 1995, Science progress.

[22]  M. Saltveit,et al.  Temperature and chemical shocks induce chilling tolerance in germinating Cucumis sativus (cv. Poinsett 76) seeds , 1994 .

[23]  R. Douce,et al.  A Low Molecular Mass Heat-Shock Protein Is Localized to Higher Plant Mitochondria , 1994, Plant physiology.

[24]  C. Guy,et al.  Structural Organization of the Spinach Endoplasmic Reticulum-Luminal 70-Kilodalton Heat-Shock Cognate Gene and Expression of 70-Kilodalton Heat-Shock Genes during Cold Acclimation , 1994, Plant physiology.

[25]  F. Salamini,et al.  Transcripts Accumulating during Cold Storage of Potato (Solanum tuberosum L.) Tubers Are Sequence Related to Stress-Responsive Genes , 1994, Plant physiology.

[26]  K. Arakawa,et al.  Cold-Induced Alterations in Plasma Membrane Proteins That are Specifically Related to the Development of Freezing Tolerance in Cold-Hardy Winter Wheat , 1994 .

[27]  M. Thomashow 30 Arabidopsis thaliana as a Model for Studying Mechanisms of Plant Cold Tolerance , 1994 .

[28]  F. Mencarelli,et al.  INFLUENCE OF HEAT TREATMENT ON THE PHYSIOLOGICAL RESPONSE OF SWEET PEPPER KEPT AT CHILLING TEMPERATURE , 1993 .

[29]  M. Gaestel,et al.  Small heat shock proteins are molecular chaperones. , 1993, The Journal of biological chemistry.

[30]  R. T. Nagao,et al.  Localization of small heat shock proteins to the higher plant endomembrane system , 1993, Molecular and cellular biology.

[31]  T. Kazuoka,et al.  Heat-stable COR (cold-regulated) proteins associated with freezing tolerance in spinach , 1992 .

[32]  C. Guy,et al.  Association of 70-kilodalton heat-shock cognate proteins with acclimation to cold. , 1992, Plant physiology.

[33]  S. Lurie,et al.  Acquisition of low-temperature tolerance in tomatoes by exposure to high-temperature stress , 1991 .

[34]  M. Saltveit,et al.  Effect of temperature conditioning on chilling injury of cucumber cotyledons: possible role of abscisic Acid and heat shock proteins. , 1991, Plant physiology.

[35]  E. Vierling The Roles of Heat Shock Proteins in Plants , 1991 .

[36]  M. Thomashow,et al.  Cold acclimation in Arabidopsis and wheat : a response associated with expression of related genes encoding ;boiling-stable' polypeptides. , 1990, Plant physiology.

[37]  L. Sticher,et al.  Heat Shock Inhibits alpha-Amylase Synthesis in Barley Aleurone without Inhibiting the Activity of Endoplasmic Reticulum Marker Enzymes. , 1990, Plant physiology.

[38]  Charles L. Guy,et al.  Cold Acclimation and Freezing Stress Tolerance: Role of Protein Metabolism , 1990 .

[39]  M. Tesche BuchbesprechungA. Sakai, W. Larcher, Frost Survival of Plants. Responses and Adaptation to Freezing Stress., Springer-Verlag, Berlin-Heidelberg-New York-LondonParis-Tokyo (1987), Series Ecological Studies 62. 321 S . , 200 Abb., zahlr. Tab. , Preis : DM 198. , 1988 .

[40]  T. Ho,et al.  Intracellular localization of heat shock proteins in maize. , 1987, Plant physiology.

[41]  A. Catesson,et al.  Changes in the membrane components of nondividing cambial cells , 1987 .

[42]  S. Yoshida Chemical and Biophysical Changes in the Plasma Membrane during Cold Acclimation of Mulberry Bark Cells (Morus bombycis Koidz. cv Goroji). , 1984, Plant physiology.

[43]  P. Steponkus Role of the Plasma Membrane in Freezing Injury and Cold Acclimation , 1984 .

[44]  A. Sakai,et al.  Ultrastructural Changes Related to Frost Hardiness in the Cortical Parenchyma Cells from Mulberry Twigs , 1981 .

[45]  J. Levitt,et al.  Responses of Plants to Environmental Stress, 2nd Edition, Volume 1: Chilling, Freezing, and High Temperature Stresses. , 1980 .

[46]  P. O’Farrell High resolution two-dimensional electrophoresis of proteins. , 1975, The Journal of biological chemistry.

[47]  P. Kramer,et al.  Responses of Plants to Environmental Stresses , 1973 .

[48]  D. Siminovitch,et al.  Seasonal cytological changes in secondary phloem parenchyma cells in Robinia pseudoacacia in relation to cold hardiness , 1971 .

[49]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[50]  A. Sakai,et al.  The role of sugar and related compounds in variations of freezing resistance. , 1968, Cryobiology.

[51]  D. Siminovitch,et al.  Phospholipid, protein, and nucleic acid increases in protoplasm and membrane structures associated with development of extreme freezing resistance in black locust tree cells. , 1968, Cryobiology.