Home LiteratureArticle Details
PMID: 17996020 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis.

The Plant journal : for cell and molecular biology ·Vol. 53 ·No. 3 ·2008-02-00 ·Pages 554-65

Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H

Abstract

Salt Overly Sensitive 1 (SOS1), a plasma membrane Na+/H+ antiporter in Arabidopsis, is a salt tolerance determinant crucial for the maintenance of ion homeostasis in saline stress conditions. SOS1 mRNA is unstable at normal growth conditions, but its stability is substantially increased under salt stress and other ionic and dehydration stresses. In addition, H2O2 treatment increases the stability of SOS1 mRNA. SOS1 mRNA is inherently unstable and rapidly degraded with a half-life of approximately 10 min. Rapid decay of SOS1 mRNA requires new protein synthesis. Stress-induced SOS1 mRNA stability is mediated by reactive oxygen species (ROS). NADPH oxidase is also involved in the upregulation of SOS1 mRNA stability, presumably through the control of extracellular ROS production. The cis-element required for SOS1 mRNA instability resides in the 500-bp region within the 2.2 kb at the 3' end of the SOS1 mRNA. Furthermore, mutations in the SOS1 gene render sos1 mutants more tolerant to paraquat, a non-selective herbicide causing oxidative stress, indicating that SOS1 plays negative roles in tolerance of oxidative stress. A hypothetical model for the signaling pathway involving SOS1-mediated pH changes, NADPH oxidase activation, apoplastic ROS production and downstream signaling transduction is proposed, and the biological significance of ROS-mediated induction of SOS1 mRNA stability is discussed.

MeSH Terms
Arabidopsis/drug effects,genetics,metabolism Arabidopsis Proteins Blotting, Northern Gene Expression Regulation, Plant/drug effects Hydrogen Peroxide/metabolism Hydrogen-Ion Concentration RNA Stability/drug effects Reactive Oxygen Species/metabolism Signal Transduction Sodium Chloride/pharmacology Sodium-Hydrogen Exchangers/genetics,metabolism
Chemicals
Arabidopsis Proteins Reactive Oxygen Species SOS1 protein, Arabidopsis Sodium-Hydrogen Exchangers Sodium Chloride Hydrogen Peroxide
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Chung Jung-Sung
Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, TX 79409, USA.
Zhu Jian-Kang
Bressan Ray A
Hasegawa Paul M
Shi Huazhong
References (54)
54 references, click to expand
  1. Repression of stress-responsive genes by FIERY2, a novel transcriptional regulator in Arabidopsis.
    Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10899-904 PMID: 12149453
  2. Posttranscriptional control of chloroplast gene expression. From RNA to photosynthetic complex.
    Plant Physiol. 2001 Jan;125(1):142-4 PMID: 11154318
  3. The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion.
    Plant Cell. 2003 Jan;15(1):19-32 PMID: 12509519
  4. Novel features of the XRN-family in Arabidopsis: evidence that AtXRN4, one of several orthologs of nuclear Xrn2p/Rat1p, functions in the cytoplasm.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13985-90 PMID: 11106401
  5. The apoplastic pH of the substomatal cavity of Vicia faba leaves and its regulation responding to different stress factors.
    J Exp Bot. 2002 Jan;53(366):73-82 PMID: 11741043
  6. mRNA degradation machines in eukaryotic cells.
    Biochimie. 2002 Aug;84(8):821-37 PMID: 12457569
  7. Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis.
    Dev Cell. 2001 Dec;1(6):771-81 PMID: 11740939
  8. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6896-901 PMID: 10823923
  9. Impacts of altered RNA metabolism on abscisic acid signaling.
    Curr Opin Plant Biol. 2003 Oct;6(5):463-9 PMID: 12972047
  10. Regulation of mRNA stability in mammalian cells.
    Gene. 2001 Mar 7;265(1-2):11-23 PMID: 11255003
  11. Paraquat-resistant cell lines derived from Chinese hamster ovary cells.
    Cell Biol Int Rep. 1990 Mar;14(3):235-46 PMID: 2160862
  12. Current perspectives on mRNA stability in plants: multiple levels and mechanisms of control.
    Trends Plant Sci. 1999 Nov;4(11):429-438 PMID: 10529824
  13. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana.
    Nat Biotechnol. 2003 Jan;21(1):81-5 PMID: 12469134
  14. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system.
    J Exp Bot. 2002 May;53(372):1367-76 PMID: 11997382
  15. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3730-4 PMID: 10725382
  16. Root-to-shoot signalling: apoplastic alkalinization, a general stress response and defence factor in barley (Hordeum vulgare).
    Protoplasma. 2005 Dec;227(1):17-24 PMID: 16389490
  17. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.
    Annu Rev Plant Biol. 2006;57:781-803 PMID: 16669782
  18. An extensive network of coupling among gene expression machines.
    Nature. 2002 Apr 4;416(6880):499-506 PMID: 11932736
  19. The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis.
    Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18816-21 PMID: 17023541
  20. Calcium at the crossroads of signaling.
    Plant Cell. 2002;14 Suppl:S401-17 PMID: 12045291
  21. Mitogen-activated protein kinases and reactive oxygen species signaling in plants.
    Plant Physiol. 2006 Jun;141(2):351-6 PMID: 16760487
  22. Signal transmission in the plant immune response.
    Trends Plant Sci. 2001 Aug;6(8):372-9 PMID: 11495791
  23. An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis.
    Cell. 2001 Aug 24;106(4):477-87 PMID: 11525733
  24. Redox cycling of the herbicide paraquat in microglial cultures.
    Brain Res Mol Brain Res. 2005 Mar 24;134(1):52-6 PMID: 15790529
  25. PLANT CELLULAR AND MOLECULAR RESPONSES TO HIGH SALINITY.
    Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:463-499 PMID: 15012199
  26. Bringing the role of mRNA decay in the control of gene expression into focus.
    Trends Genet. 2004 Oct;20(10):491-7 PMID: 15363903
  27. The expanding family of eucaryotic Na(+)/H(+) exchangers.
    J Biol Chem. 2000 Jan 7;275(1):1-4 PMID: 10617577
  28. The cap-to-tail guide to mRNA turnover.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):237-46 PMID: 11283721
  29. The origin of the oxidative burst in plants.
    Free Radic Res. 1995 Dec;23(6):517-32 PMID: 8574346
  30. Reactive oxygen species: metabolism, oxidative stress, and signal transduction.
    Annu Rev Plant Biol. 2004;55:373-99 PMID: 15377225
  31. RNA-binding proteins in plants: the tip of an iceberg?
    Curr Opin Plant Biol. 2002 Oct;5(5):452-9 PMID: 12183185
  32. The control of mRNA stability in response to extracellular stimuli.
    Mol Cells. 2002 Dec 31;14(3):323-31 PMID: 12521293
  33. The role of microglia in paraquat-induced dopaminergic neurotoxicity.
    Antioxid Redox Signal. 2005 May-Jun;7(5-6):654-61 PMID: 15890010
  34. A calcium sensor homolog required for plant salt tolerance.
    Science. 1998 Jun 19;280(5371):1943-5 PMID: 9632394
  35. Salt and drought stress signal transduction in plants.
    Annu Rev Plant Biol. 2002;53:247-73 PMID: 12221975
  36. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs.
    Plant Cell. 1998 Feb;10(2):255-66 PMID: 9490748
  37. The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants.
    Plant Cell. 2002 Feb;14(2):465-77 PMID: 11884687
  38. The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance.
    Plant Cell. 2002 Mar;14(3):575-88 PMID: 11910005
  39. Coupling transcription, splicing and mRNA export.
    Curr Opin Cell Biol. 2003 Jun;15(3):326-31 PMID: 12787775
  40. Emerging MAP kinase pathways in plant stress signalling.
    Trends Plant Sci. 2005 Jul;10(7):339-46 PMID: 15953753
  41. Mutants of Arabidopsis defective in a sequence-specific mRNA degradation pathway.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13991-6 PMID: 11087822
  42. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.
    Curr Opin Plant Biol. 2005 Aug;8(4):397-403 PMID: 15939662
  43. C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development.
    Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10893-8 PMID: 12149434
  44. Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants.
    Planta. 2005 Dec;222(6):1041-50 PMID: 16079998
  45. Recent advances in understanding the origin of the apoplastic oxidative burst in plant cells.
    Free Radic Res. 1999 Dec;31 Suppl:S137-45 PMID: 10694052
  46. Production of reactive oxygen species by plant NADPH oxidases.
    Plant Physiol. 2006 Jun;141(2):336-40 PMID: 16760484
  47. Apoplastic pH signaling in barley leaves attacked by the powdery mildew fungus Blumeria graminis f. sp. hordei.
    Mol Plant Microbe Interact. 2004 Jan;17(1):118-23 PMID: 14714875
  48. Colour-enhancing protein in blue petals.
    Nature. 2000 Oct 5;407(6804):581 PMID: 11034195
  49. Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection.
    Plant Physiol. 2001 Jul;126(3):1281-90 PMID: 11457979
  50. Elicitor signal transduction leading to production of plant secondary metabolites.
    Biotechnol Adv. 2005 Jun;23(4):283-333 PMID: 15848039
  51. Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase.
    Nature. 2002 Aug 15;418(6899):793-7 PMID: 12181571
  52. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.
    Nature. 2003 Mar 27;422(6930):442-6 PMID: 12660786
  53. 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
  54. Hydrogen peroxide mediates plant root cell response to nutrient deprivation.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8827-32 PMID: 15173595
Article Info
Journal
The Plant journal : for cell and molecular biology
Abbr.
Plant J
ISSN
0960-7412
DOI
10.1111/j.1365-313X.2007.03364.x
Published
2008-02-00
Epub
2007-00-07
Pages
554-65
Language
English
Region
England
NLM ID
9207397
PMCID
PMC3128381
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059138 · United States
NIGMS NIH HHS · R01 GM059138-15 · United States
External Links
PubMed source DOI: 10.1111/j.1365-313X.2007.03364.x PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2