Home LiteratureArticle Details
PMID: 20195524 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Salt stress causes peroxisome proliferation, but inducing peroxisome proliferation does not improve NaCl tolerance in Arabidopsis thaliana.

PloS one ·Vol. 5 ·No. 2 ·2010-02-24 ·Pages e9408

Mitsuya S, El-Shami M, Sparkes IA, Charlton WL, Lousa Cde M, Johnson B, Baker A

Abstract

The PEX11 family of peroxisome membrane proteins have been shown to be involved in regulation of peroxisome size and number in plant, animals, and yeast cells. We and others have previously suggested that peroxisome proliferation as a result of abiotic stress may be important in plant stress responses, and recently it was reported that several rice PEX11 genes were up regulated in response to abiotic stress. We sought to test the hypothesis that promoting peroxisome proliferation in Arabidopsis thaliana by over expression of one PEX11 family member, PEX11e, would give increased resistance to salt stress. We could demonstrate up regulation of PEX11e by salt stress and increased peroxisome number by both PEX11e over expression and salt stress, however our experiments failed to find a correlation between PEX11e over expression and increased peroxisome metabolic activity or resistance to salt stress. This suggests that although peroxisome proliferation may be a consequence of salt stress, it does not affect the ability of Arabidopsis plants to tolerate saline conditions.

MeSH Terms
Arabidopsis/cytology,genetics,physiology Arabidopsis Proteins/genetics,metabolism,physiology Cell Line Cells, Cultured Gene Expression Regulation, Plant/drug effects Immunoblotting Luminescent Proteins/genetics,metabolism Membrane Proteins/genetics,metabolism,physiology Microscopy, Fluorescence Peroxins Peroxisomes/drug effects,metabolism,physiology Plants, Genetically Modified Protein Isoforms/genetics,metabolism,physiology Salt Tolerance/physiology Sodium Chloride/pharmacology Tobacco/cytology Up-Regulation/drug effects
Chemicals
Arabidopsis Proteins Luminescent Proteins Membrane Proteins Peroxins Protein Isoforms peroxin 11 protein, Arabidopsis Sodium Chloride
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Mitsuya Shiro
Centre for Plant Sciences, University of Leeds, Leeds, United Kingdom.
El-Shami Mahmoud
Sparkes Imogen A
Charlton Wayne L
Lousa Carine De Marcos
Johnson Barbara
Baker Alison
References (59)
59 references, click to expand
  1. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23 PMID: 10737809
  2. The biochemistry of oleate induction: transcriptional upregulation and peroxisome proliferation.
    Biochim Biophys Acta. 2006 Dec;1763(12):1392-402 PMID: 16949166
  3. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation.
    Plant Cell. 2002 Jun;14(6):1405-15 PMID: 12084835
  4. Arabidopsis PEROXIN11c-e, FISSION1b, and DYNAMIN-RELATED PROTEIN3A cooperate in cell cycle-associated replication of peroxisomes.
    Plant Cell. 2008 Jun;20(6):1567-85 PMID: 18539750
  5. FISSION1A and FISSION1B proteins mediate the fission of peroxisomes and mitochondria in Arabidopsis.
    Mol Plant. 2008 Nov;1(6):1036-47 PMID: 19825601
  6. In vivo interaction between atToc33 and atToc159 GTP-binding domains demonstrated in a plant split-ubiquitin system.
    J Exp Bot. 2009;60(1):257-67 PMID: 19010773
  7. MADS-box protein complexes control carpel and ovule development in Arabidopsis.
    Plant Cell. 2003 Nov;15(11):2603-11 PMID: 14555696
  8. Pex30p, Pex31p, and Pex32p form a family of peroxisomal integral membrane proteins regulating peroxisome size and number in Saccharomyces cerevisiae.
    Mol Biol Cell. 2004 Feb;15(2):665-77 PMID: 14617799
  9. Light induces peroxisome proliferation in Arabidopsis seedlings through the photoreceptor phytochrome A, the transcription factor HY5 HOMOLOG, and the peroxisomal protein PEROXIN11b.
    Plant Physiol. 2008 Mar;146(3):1117-27 PMID: 18203870
  10. Two small protein families, DYNAMIN-RELATED PROTEIN3 and FISSION1, are required for peroxisome fission in Arabidopsis.
    Plant J. 2009 Jan;57(1):146-59 PMID: 18785999
  11. Arabidopsis 22-kilodalton peroxisomal membrane protein. Nucleotide sequence analysis and biochemical characterization.
    Plant Physiol. 1999 May;120(1):309-20 PMID: 10318708
  12. Pmp27 promotes peroxisomal proliferation.
    J Cell Biol. 1995 Apr;129(2):345-55 PMID: 7721939
  13. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  14. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11.
    J Biol Chem. 2003 May 9;278(19):17012-20 PMID: 12618434
  15. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants.
    Nat Protoc. 2006;1(4):2019-25 PMID: 17487191
  16. The ER-peroxisome connection in plants: development of the "ER semi-autonomous peroxisome maturation and replication" model for plant peroxisome biogenesis.
    Biochim Biophys Acta. 2006 Dec;1763(12):1655-68 PMID: 17049631
  17. PEX11 beta deficiency is lethal and impairs neuronal migration but does not abrogate peroxisome function.
    Mol Cell Biol. 2002 Jun;22(12):4358-65 PMID: 12024045
  18. Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants.
    Plant Cell Physiol. 2007 Jun;48(6):763-74 PMID: 17478547
  19. Increased levels of peroxisomal active oxygen-related enzymes in copper-tolerant pea plants.
    Plant Physiol. 1987 Oct;85(2):570-4 PMID: 16665737
  20. Salt and drought stress signal transduction in plants.
    Annu Rev Plant Biol. 2002;53:247-73 PMID: 12221975
  21. An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division.
    Plant J. 2004 May;38(3):487-98 PMID: 15086806
  22. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2117-27 PMID: 15258265
  23. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray.
    Plant J. 2002 Aug;31(3):279-92 PMID: 12164808
  24. Chewing the fat: beta-oxidation in signalling and development.
    Trends Plant Sci. 2006 Mar;11(3):124-32 PMID: 16490379
  25. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
    Plant Physiol. 2004 Sep;136(1):2621-32 PMID: 15375207
  26. The JAZ family of repressors is the missing link in jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):666-71 PMID: 17637675
  27. Conserved function of pex11p and the novel pex25p and pex27p in peroxisome biogenesis.
    Mol Biol Cell. 2003 Oct;14(10):4316-28 PMID: 14517338
  28. Pex3p initiates the formation of a preperoxisomal compartment from a subdomain of the endoplasmic reticulum in Saccharomyces cerevisiae.
    J Biol Chem. 2005 Oct 14;280(41):34933-9 PMID: 16087670
  29. Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain.
    Plant J. 1997 Mar;11(3):513-23 PMID: 9107039
  30. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein.
    Plant Cell. 1998 Jun;10(6):1043-54 PMID: 9634591
  31. Isolation of the Arabidopsis ABI3 gene by positional cloning.
    Plant Cell. 1992 Oct;4(10):1251-61 PMID: 1359917
  32. Plant peroxisomes as a source of signalling molecules.
    Biochim Biophys Acta. 2006 Dec;1763(12):1478-95 PMID: 17030442
  33. Shuttles and cycles: transport of proteins into the peroxisome matrix (review).
    Mol Membr Biol. 2008 Aug;25(5):363-75 PMID: 18651315
  34. Storage of competent cells for Agrobacterium transformation.
    Nucleic Acids Res. 1988 Oct 25;16(20):9877 PMID: 3186459
  35. Nature of the hepatomegalic effect produced by ethyl-chlorophenoxy-isobutyrate in the rat.
    Nature. 1965 Nov 27;208(5013):856-8 PMID: 5870099
  36. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis.
    Plant Cell. 2004 Jul;16(7):1938-50 PMID: 15208388
  37. Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p.
    J Cell Biol. 1995 Feb;128(4):509-23 PMID: 7860627
  38. Maintaining peroxisome populations: a story of division and inheritance.
    Annu Rev Cell Dev Biol. 2007;23:321-44 PMID: 17506702
  39. Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation.
    J Cell Sci. 2006 May 1;119(Pt 9):1961-72 PMID: 16636080
  40. YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size, and distribution in Saccharomyces cerevisiae.
    J Cell Biol. 2003 Apr 28;161(2):321-32 PMID: 12707309
  41. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):661-5 PMID: 17637677
  42. Comprehensive sequence and expression profile analysis of PEX11 gene family in rice.
    Gene. 2008 Apr 15;412(1-2):59-70 PMID: 18291602
  43. Shared components of mitochondrial and peroxisomal division.
    Biochim Biophys Acta. 2006 May-Jun;1763(5-6):531-41 PMID: 16487606
  44. PEX11alpha is required for peroxisome proliferation in response to 4-phenylbutyrate but is dispensable for peroxisome proliferator-activated receptor alpha-mediated peroxisome proliferation.
    Mol Cell Biol. 2002 Dec;22(23):8226-40 PMID: 12417726
  45. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction.
    Plant Cell. 1997 May;9(5):759-71 PMID: 9165752
  46. Contribution of the endoplasmic reticulum to peroxisome formation.
    Cell. 2005 Jul 15;122(1):85-95 PMID: 16009135
  47. Fis1, DLP1, and Pex11p coordinately regulate peroxisome morphogenesis.
    Exp Cell Res. 2007 May 1;313(8):1675-86 PMID: 17408615
  48. AtPEX2 and AtPEX10 are targeted to peroxisomes independently of known endoplasmic reticulum trafficking routes.
    Plant Physiol. 2005 Oct;139(2):690-700 PMID: 16169966
  49. Mutations in the Arabidopsis peroxisomal ABC transporter COMATOSE allow differentiation between multiple functions in planta: insights from an allelic series.
    Mol Biol Cell. 2009 Jan;20(1):530-43 PMID: 19019987
  50. Peroxisome proliferation and oxidative stress mediated by activated oxygen species in plant peroxisomes.
    Arch Biochem Biophys. 1991 May 15;287(1):68-74 PMID: 1897996
  51. Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation.
    FEBS J. 2005 Oct;272(20):5169-81 PMID: 16218949
  52. The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis.
    Plant Cell. 2007 Jan;19(1):333-50 PMID: 17220199
  53. The significance of peroxisomes in methanol metabolism in methylotrophic yeast.
    Biochim Biophys Acta. 2006 Dec;1763(12):1453-62 PMID: 17023065
  54. Pex11-related proteins in peroxisome dynamics: a role for the novel peroxin Pex27p in controlling peroxisome size and number in Saccharomyces cerevisiae.
    Mol Biol Cell. 2003 Oct;14(10):4089-102 PMID: 14517321
  55. Redox-sensitive homodimerization of Pex11p: a proposed mechanism to regulate peroxisomal division.
    J Cell Biol. 1996 Oct;135(1):123-37 PMID: 8858168
  56. Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling.
    Plant Physiol. 2006 Jun;141(2):330-5 PMID: 16760483
  57. The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER.
    J Cell Biol. 2006 May 22;173(4):521-32 PMID: 16717127
  58. Expression of PEX11beta mediates peroxisome proliferation in the absence of extracellular stimuli.
    J Biol Chem. 1998 Nov 6;273(45):29607-14 PMID: 9792670
  59. Relay and control of abscisic acid signaling.
    Curr Opin Plant Biol. 2003 Oct;6(5):470-9 PMID: 12972048
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2010-02-24
Epub
2010-00-24
Pages
e9408
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC2827565
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/D524875/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · 24/P13265 · United Kingdom
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]