Home LiteratureArticle Details
PMID: 15208400 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis.

The Plant cell ·Vol. 16 ·No. 7 ·2004-07-00 ·Pages 1912-24

Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D'Angelo C, Weinl S, Kudla J, Luan S

Abstract

Calcium plays a pivotal role in plant responses to several stimuli, including pathogens, abiotic stresses, and hormones. However, the molecular mechanisms underlying calcium functions are poorly understood. It is hypothesized that calcium serves as second messenger and, in many cases, requires intracellular protein sensors to transduce the signal further downstream in the pathways. The calcineurin B-like proteins (CBLs) represent a unique family of calcium sensors in plant cells. Here, we report our analysis of the CBL9 member of this gene family. Expression of CBL9 was inducible by multiple stress signals and abscisic acid (ABA) in young seedlings. When CBL9 gene function was disrupted in Arabidopsis thaliana plants, the responses to ABA were drastically altered. The mutant plants became hypersensitive to ABA in the early developmental stages, including seed germination and post-germination seedling growth. In addition, seed germination in the mutant also showed increased sensitivity to inhibition by osmotic stress conditions produced by high concentrations of salt and mannitol. Further analyses indicated that increased stress sensitivity in the mutant may be a result of both ABA hypersensitivity and increased accumulation of ABA under the stress conditions. The cbl9 mutant plants showed enhanced expression of genes involved in ABA signaling, such as ABA-INSENSITIVE 4 and 5. This study has identified a calcium sensor as a common element in the ABA signaling and stress-induced ABA biosynthesis pathways.

MeSH Terms
Abscisic Acid/metabolism Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Calcium-Binding Proteins/metabolism Culture Media Gene Expression Regulation, Plant Germination Glucose/metabolism Mannitol/metabolism Molecular Sequence Data Mutation Osmotic Pressure Plants, Genetically Modified Seeds/growth & development,metabolism Signal Transduction Sodium Chloride/metabolism
Chemicals
Arabidopsis Proteins Calcium-Binding Proteins Culture Media calcineurin B-like protein 1, Arabidopsis Mannitol Sodium Chloride Abscisic Acid Glucose
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Pandey Girdhar K
Department of Plant and Microbial Biology, University of California, Berkeley 94720, USA.
Cheong Yong Hwa
Kim Kyung-Nam
Grant John J
Li Legong
Hung Wendy
D'Angelo Cecilia
Weinl Stefan
Kudla Jörg
Luan Sheng
References (48)
48 references, click to expand
  1. The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh.
    Plant Mol Biol. 1992 Dec;20(5):951-62 PMID: 1463831
  2. Systematic reverse genetics of transfer-DNA-tagged lines of Arabidopsis. Isolation of mutations in the cytochrome p450 gene superfamily.
    Plant Physiol. 1998 Nov;118(3):743-50 PMID: 9808718
  3. Constitutive activation and transgenic evaluation of the function of an arabidopsis PKS protein kinase.
    J Biol Chem. 2002 Nov 1;277(44):42088-96 PMID: 12198122
  4. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks.
    Plant Physiol. 2004 Jan;134(1):43-58 PMID: 14730064
  5. Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana.
    Plant Mol Biol. 1992 Jul;19(4):689-92 PMID: 1627780
  6. Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15812-7 PMID: 12434021
  7. Calcium at the crossroads of signaling.
    Plant Cell. 2002;14 Suppl:S401-17 PMID: 12045291
  8. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4718-23 PMID: 10200328
  9. The calcium sensor CBL1 integrates plant responses to abiotic stresses.
    Plant J. 2003 Nov;36(4):457-70 PMID: 14617077
  10. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  11. Abscisic acid signaling in seeds and seedlings.
    Plant Cell. 2002;14 Suppl:S15-45 PMID: 12045268
  12. Communicating with calcium
    Plant Cell. 1999 Apr;11(4):691-706 PMID: 10213787
  13. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells.
    Plant Cell. 1999 Sep;11(9):1785-98 PMID: 10488243
  14. Biochemical and functional characterization of PKS11, a novel Arabidopsis protein kinase.
    J Biol Chem. 2002 Aug 2;277(31):28340-50 PMID: 12029080
  15. Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome.
    Plant Cell Environ. 2002 Feb;25(2):153-161 PMID: 11841660
  16. Regulation of abscisic acid biosynthesis.
    Plant Physiol. 2003 Sep;133(1):29-36 PMID: 12970472
  17. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis.
    Plant Cell. 2003 Feb;15(2):411-23 PMID: 12566581
  18. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.
    Curr Opin Plant Biol. 2000 Jun;3(3):217-23 PMID: 10837265
  19. cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana.
    Plant Mol Biol. 1992 Jan;18(1):13-21 PMID: 1731964
  20. Abscisic acid signaling.
    Curr Opin Cell Biol. 1995 Apr;7(2):232-8 PMID: 7612276
  21. Abiotic stress signalling pathways: specificity and cross-talk.
    Trends Plant Sci. 2001 Jun;6(6):262-7 PMID: 11378468
  22. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  23. CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis.
    Plant Cell. 2003 Aug;15(8):1833-45 PMID: 12897256
  24. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants.
    Plant Cell. 2002;14 Suppl:S389-400 PMID: 12045290
  25. ABSCISIC ACID SIGNAL TRANSDUCTION.
    Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:199-222 PMID: 15012233
  26. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis.
    Dev Cell. 2002 Aug;3(2):233-44 PMID: 12194854
  27. CDPKs - a kinase for every Ca2+ signal?
    Trends Plant Sci. 2000 Apr;5(4):154-9 PMID: 10740296
  28. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells.
    Plant Cell. 1996 Feb;8(2):259-69 PMID: 8742711
  29. Signal Transduction in Barley Aleurone Protoplasts Is Calcium Dependent and Independent.
    Plant Cell. 1996 Dec;8(12):2193-2209 PMID: 12239376
  30. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress.
    Plant Cell. 1994 Feb;6(2):251-64 PMID: 8148648
  31. Ca2+-dependent protein kinases and stress signal transduction in plants.
    Science. 1996 Dec 13;274(5294):1900-2 PMID: 8943201
  32. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants.
    Plant Cell. 1997 Mar;9(3):409-23 PMID: 9090884
  33. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance.
    Science. 1998 Apr 3;280(5360):104-6 PMID: 9525853
  34. Cross-talk in abscisic acid signaling.
    Sci STKE. 2002 Jul 9;2002(140):re10 PMID: 12107340
  35. Cell signaling during cold, drought, and salt stress.
    Plant Cell. 2002;14 Suppl:S165-83 PMID: 12045276
  36. The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium.
    Planta. 1997 Dec;203(4):442-7 PMID: 9421928
  37. Complex regulation of ABA biosynthesis in plants.
    Trends Plant Sci. 2002 Jan;7(1):41-8 PMID: 11804826
  38. Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis.
    J Exp Bot. 2000 Oct;51(351):1679-86 PMID: 11053457
  39. Three genes that affect sugar sensing (abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1) are differentially regulated by glucose in Arabidopsis.
    Plant Physiol. 2003 Sep;133(1):231-42 PMID: 12970489
  40. The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression.
    Plant Cell. 2001 Sep;13(9):2063-83 PMID: 11549764
  41. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.
    Plant Cell. 1998 Aug;10(8):1391-406 PMID: 9707537
  42. CALMODULIN AND CALMODULIN-BINDING PROTEINS IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:697-725 PMID: 15012251
  43. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4782-7 PMID: 11287670
  44. A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin.
    Plant Cell. 2000 Dec;12(12):2351-2366 PMID: 11148283
  45. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation.
    Plant Cell. 1996 Mar;8(3):489-503 PMID: 8721751
  46. An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis.
    Plant Cell. 2002 May;14(5):1109-20 PMID: 12034900
  47. Relay and control of abscisic acid signaling.
    Curr Opin Plant Biol. 2003 Oct;6(5):470-9 PMID: 12972048
  48. Calcium signalling in Arabidopsis thaliana responding to drought and salinity.
    Plant J. 1997 Nov;12(5):1067-78 PMID: 9418048
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-07-00
Epub
2004-00-18
Pages
1912-24
Language
English
Region
England
NLM ID
9208688
PMCID
PMC514170
Subset
IM
Databases
GENBANK
AF411958
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]