Home LiteratureArticle Details
PMID: 11457955 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress.

Plant physiology ·Vol. 126 ·No. 3 ·2001-07-00 ·Pages 1042-54

Alvim FC, Carolino SM, Cascardo JC, Nunes CC, Martinez CA, Otoni WC, Fontes EP

Abstract

The binding protein (BiP) is an important component of endoplasmic reticulum stress response of cells. Despite extensive studies in cultured cells, a protective function of BiP against stress has not yet been demonstrated in whole multicellular organisms. Here, we have obtained transgenic tobacco (Nicotiana tabacum L. cv Havana) plants constitutively expressing elevated levels of BiP or its antisense cDNA to analyze the protective role of this endoplasmic reticulum lumenal stress protein at the whole plant level. Elevated levels of BiP in transgenic sense lines conferred tolerance to the glycosylation inhibitor tunicamycin during germination and tolerance to water deficit during plant growth. Under progressive drought, the leaf BiP levels correlated with the maintenance of the shoot turgidity and water content. The protective effect of BiP overexpression against water stress was disrupted by expression of an antisense BiP cDNA construct. Although overexpression of BiP prevented cellular dehydration, the stomatal conductance and transpiration rate in droughted sense leaves were higher than in control and antisense leaves. The rate of photosynthesis under water deficit might have caused a degree of greater osmotic adjustment in sense leaves because it remained unaffected during water deprivation, which was in marked contrast with the severe drought-induced decrease in the CO(2) assimilation in control and antisense leaves. In antisense plants, the water stress stimulation of the antioxidative defenses was higher than in control plants, whereas in droughted sense leaves an induction of superoxide dismutase activity was not observed. These results suggest that overexpression of BiP in plants may prevent endogenous oxidative stress.

MeSH Terms
Adaptation, Physiological Arabidopsis Proteins Carrier Proteins/genetics,metabolism,physiology Endoplasmic Reticulum/physiology Enzyme Induction Fresh Water Genes, Plant Germination/drug effects Oxidative Stress Plant Leaves/physiology Plant Proteins/genetics,metabolism,physiology Plant Shoots/physiology Plants, Genetically Modified Plants, Toxic Seeds/drug effects Soybeans/genetics Tobacco/enzymology,genetics,physiology Tunicamycin/pharmacology
Chemicals
Arabidopsis Proteins Carrier Proteins Plant Proteins Tunicamycin BIP protein, Arabidopsis
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Alvim F C
Departamento de Biologia Vegetal, BIOAGRO-Universidade Federal de Viçosa, 36571.000 Viçosa, Minas Gerais, Brazil.
Carolino S M
Cascardo J C
Nunes C C
Martinez C A
Otoni W C
Fontes E P
References (45)
45 references, click to expand
  1. 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.
    Plant Physiol. 1994 Apr;104(4):1359-70 PMID: 8016266
  2. tRNA ligase is required for regulated mRNA splicing in the unfolded protein response.
    Cell. 1996 Nov 1;87(3):405-13 PMID: 8898194
  3. Protein changes in response to progressive water deficit in maize . Quantitative variation and polypeptide identification
    Plant Physiol. 1998 Aug;117(4):1253-63 PMID: 9701581
  4. Establishment of a Chinese hamster ovary cell line that expresses grp78 antisense transcripts and suppresses A23187 induction of both GRP78 and GRP94.
    J Cell Physiol. 1992 Dec;153(3):575-82 PMID: 1332981
  5. Mouse lymphoma cells destined to undergo apoptosis in response to thapsigargin treatment fail to generate a calcium-mediated grp78/grp94 stress response.
    J Biol Chem. 1997 Feb 28;272(9):6087-92 PMID: 9038234
  6. Suppression of stress protein GRP78 induction in tumor B/C10ME eliminates resistance to cell mediated cytotoxicity.
    Cancer Res. 1993 Dec 15;53(24):6001-5 PMID: 8261413
  7. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  8. Glucose regulated protein induction and cellular resistance to oxidative stress mediated by porphyrin photosensitization.
    Cancer Res. 1991 Dec 15;51(24):6574-9 PMID: 1835901
  9. Bean homologs of the mammalian glucose-regulated proteins: induction by tunicamycin and interaction with newly synthesized seed storage proteins in the endoplasmic reticulum.
    Plant J. 1992 Jul;2(4):443-55 PMID: 1344885
  10. Protein determination using bicinchoninic acid in the presence of sulfhydryl reagents.
    Anal Biochem. 1988 Apr;170(1):203-8 PMID: 3389511
  11. Sensitivity of cell division and cell elongation to low water potentials in soybean hypocotyls.
    Planta. 1972 Mar;108(1):77-87 PMID: 24473747
  12. Endoplasmic reticulum stress proteins block oxidant-induced Ca2+ increases and cell death.
    J Biol Chem. 1998 May 22;273(21):12858-62 PMID: 9582315
  13. Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs.
    Planta. 1995;195(4):611-21 PMID: 7766051
  14. The endoplasmic reticulum of plant cells and its role in protein maturation and biogenesis of oil bodies.
    Plant Mol Biol. 1998 Sep;38(1-2):1-29 PMID: 9738958
  15. The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo.
    Plant Cell. 1995 Apr;7(4):391-406 PMID: 7773014
  16. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response.
    Cell. 1997 Sep 19;90(6):1031-9 PMID: 9323131
  17. Gene Expression and Signal Transduction in Water-Stress Response.
    Plant Physiol. 1997 Oct;115(2):327-334 PMID: 12223810
  18. Endoplasmic reticulum chaperones GRP78 and calreticulin prevent oxidative stress, Ca2+ disturbances, and cell death in renal epithelial cells.
    J Biol Chem. 1997 Aug 29;272(35):21751-9 PMID: 9268304
  19. The dynamic role of GRP78/BiP in the coordination of mRNA translation with protein processing.
    J Biol Chem. 1999 Jan 1;274(1):486-93 PMID: 9867869
  20. Superoxide dismutases: I. Occurrence in higher plants.
    Plant Physiol. 1977 Feb;59(2):309-14 PMID: 16659839
  21. The phosphorylation state and expression of soybean BiP isoforms are differentially regulated following abiotic stresses.
    J Biol Chem. 2000 May 12;275(19):14494-500 PMID: 10799532
  22. Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant.
    Plant Cell. 1991 May;3(5):483-96 PMID: 1840923
  23. Cloning of mammalian Ire1 reveals diversity in the ER stress responses.
    EMBO J. 1998 Oct 1;17(19):5708-17 PMID: 9755171
  24. The current state of two-dimensional electrophoresis with immobilized pH gradients.
    Electrophoresis. 1988 Sep;9(9):531-46 PMID: 3072185
  25. Competitive inhibition of a set of endoplasmic reticulum protein genes (GRP78, GRP94, and ERp72) retards cell growth and lowers viability after ionophore treatment.
    Mol Cell Biol. 1991 Jul;11(7):3446-53 PMID: 2046663
  26. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus.
    Cell. 1993 Aug 27;74(4):743-56 PMID: 8358794
  27. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response.
    Cell. 1996 Nov 1;87(3):391-404 PMID: 8898193
  28. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus.
    EMBO J. 1996 Jun 17;15(12):3028-39 PMID: 8670804
  29. Mammalian stress response: induction of the glucose-regulated protein family.
    Curr Opin Cell Biol. 1992 Apr;4(2):267-73 PMID: 1599691
  30. A simple, reproducible and cheap batch method for the analysis of serum glycoproteins using sepharose-coupled lectins and silver staining.
    Clin Chim Acta. 1987 Aug 14;167(2):217-23 PMID: 3665096
  31. A defective signal peptide in the maize high-lysine mutant floury 2.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6828-31 PMID: 7624327
  32. Calcium-sensitive transcriptional activation of the proximal CCAAT regulatory element of the grp78/BiP promoter by the human nuclear factor CBF/NF-Y.
    J Biol Chem. 1996 Nov 15;271(46):28995-9002 PMID: 8910550
  33. Molecular chaperones and protein folding in plants.
    Plant Mol Biol. 1996 Oct;32(1-2):191-222 PMID: 8980480
  34. Increased expression of the maize immunoglobulin binding protein homolog b-70 in three zein regulatory mutants.
    Plant Cell. 1991 May;3(5):497-505 PMID: 1840924
  35. A defective signal peptide tethers the floury-2 zein to the endoplasmic reticulum membrane.
    Plant Physiol. 1997 May;114(1):345-52 PMID: 9159955
  36. Quality control in the secretory pathway.
    Curr Opin Cell Biol. 1995 Aug;7(4):523-9 PMID: 7495572
  37. Osmoregulation, solute distribution, and growth in soybean seedlings having low water potentials.
    Planta. 1981 May;151(5):482-9 PMID: 24302115
  38. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  39. Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins.
    J Biol Chem. 1997 Feb 14;272(7):4327-34 PMID: 9020152
  40. BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+.
    J Biol Chem. 1997 Dec 5;272(49):30873-9 PMID: 9388233
  41. Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress.
    Plant Cell. 1999 Mar;11(3):459-70 PMID: 10072404
  42. THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:377-403 PMID: 15012294
  43. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene.
    Cell. 1989 Jun 30;57(7):1211-21 PMID: 2661018
  44. Generation of a mammalian cell line deficient in glucose-regulated protein stress induction through targeted ribozyme driven by a stress-inducible promoter.
    J Biol Chem. 1995 Apr 21;270(16):9526-34 PMID: 7721881
  45. A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins.
    EMBO J. 1992 Jul;11(7):2583-93 PMID: 1628622
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2001-07-00
Pages
1042-54
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC116461
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]