Home LiteratureArticle Details
PMID: 21173023 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis.

Plant physiology ·Vol. 155 ·No. 2 ·2011-02-00 ·Pages 797-807

Hirano T, Matsuzawa T, Takegawa K, Sato MH

Abstract

In eukaryotic cells, PtdIns 3,5-kinase, Fab1/PIKfyve produces PtdIns (3,5) P(2) from PtdIns 3-P, and functions in vacuole/lysosome homeostasis. Herein, we show that expression of Arabidopsis (Arabidopsis thaliana) FAB1A/B in fission yeast (Schizosaccharomyces pombe) fab1 knockout cells fully complements the vacuole morphology phenotype. Subcellular localizations of FAB1A and FAB1B fused with green fluorescent protein revealed that FAB1A/B-green fluorescent proteins localize to the endosomes in root epidermal cells of Arabidopsis. Furthermore, reduction in the expression levels of FAB1A/B by RNA interference impairs vacuolar acidification and endocytosis. These results indicate that Arabidopsis FAB1A/B functions as PtdIns 3,5-kinase in plants and in fission yeast. Conditional knockdown mutant shows various phenotypes including root growth inhibition, hyposensitivity to exogenous auxin, and disturbance of root gravitropism. These phenotypes are observed also in the overproducing mutants of FAB1A and FAB1B. The overproducing mutants reveal additional morphological phenotypes including dwarfism, male-gametophyte sterility, and abnormal floral organs. Taken together, this evidence indicates that imbalanced expression of FAB1A/B impairs endomembrane homeostasis including endocytosis, vacuole formation, and vacuolar acidification, which causes pleiotropic developmental phenotypes mostly related to the auxin signaling in Arabidopsis.

MeSH Terms
Arabidopsis/cytology,enzymology,genetics Arabidopsis Proteins/genetics Cell Membrane/physiology Endosomes/physiology Gene Knockdown Techniques Genetic Complementation Test Gravitropism Homeostasis Indoleacetic Acids/pharmacology Mutation Phosphotransferases (Alcohol Group Acceptor)/genetics Plant Infertility Plant Roots/growth & development Plants, Genetically Modified/cytology,enzymology,genetics RNA, Plant/genetics Schizosaccharomyces/genetics,metabolism Vacuoles/metabolism
Chemicals
Arabidopsis Proteins Indoleacetic Acids RNA, Plant FAB1A protein, Arabidopsis FAB1B protein, Arabidopsis Phosphotransferases (Alcohol Group Acceptor)
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hirano Tomoko
Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan.
Matsuzawa Tomohiko
Takegawa Kaoru
Sato Masa H
References (30)
30 references, click to expand
  1. Gene silencing in plants using artificial microRNAs and other small RNAs.
    Plant J. 2008 Feb;53(4):674-90 PMID: 18269576
  2. Complementation analysis in PtdInsP kinase-deficient yeast mutants demonstrates that Schizosaccharomyces pombe and murine Fab1p homologues are phosphatidylinositol 3-phosphate 5-kinases.
    J Biol Chem. 1999 Nov 26;274(48):33905-12 PMID: 10567352
  3. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  4. The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation.
    Plant J. 1995 Feb;7(2):211-20 PMID: 7704045
  5. Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen.
    Plant Physiol. 2009 Dec;151(4):1812-22 PMID: 19846542
  6. Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1.
    Plant Cell. 2004 Nov;16(11):3069-83 PMID: 15486104
  7. Phosphatidylinositol 3-phosphate 5-kinase is required for the cellular response to nutritional starvation and mating pheromone signals in Schizosaccharomyces pombe.
    Genes Cells. 2002 Feb;7(2):199-215 PMID: 11895483
  8. Core protein machinery for mammalian phosphatidylinositol 3,5-bisphosphate synthesis and turnover that regulates the progression of endosomal transport. Novel Sac phosphatase joins the ArPIKfyve-PIKfyve complex.
    J Biol Chem. 2007 Aug 17;282(33):23878-91 PMID: 17556371
  9. Atg18 regulates organelle morphology and Fab1 kinase activity independent of its membrane recruitment by phosphatidylinositol 3,5-bisphosphate.
    Mol Biol Cell. 2007 Nov;18(11):4232-44 PMID: 17699591
  10. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve.
    J Biol Chem. 2001 Jul 13;276(28):26141-7 PMID: 11285266
  11. The Fab1 phosphatidylinositol kinase pathway in the regulation of vacuole morphology.
    Curr Opin Cell Biol. 2005 Aug;17(4):402-8 PMID: 15975782
  12. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis.
    J Cell Biol. 1998 Oct 5;143(1):65-79 PMID: 9763421
  13. A protein complex that regulates PtdIns(3,5)P2 levels.
    EMBO J. 2009 Jan 21;28(2):86-7 PMID: 19158662
  14. Thiamine-repressible expression vectors pREP and pRIP for fission yeast.
    Gene. 1993 Jan 15;123(1):127-30 PMID: 8422996
  15. Highly specific gene silencing by artificial microRNAs in Arabidopsis.
    Plant Cell. 2006 May;18(5):1121-33 PMID: 16531494
  16. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis.
    Plant Physiol. 2003 Jun;132(2):530-43 PMID: 12805585
  17. Complex regulation of Arabidopsis AGR1/PIN2-mediated root gravitropic response and basipetal auxin transport by cantharidin-sensitive protein phosphatases.
    Plant J. 2005 Apr;42(2):188-200 PMID: 15807782
  18. Comparative analysis of the MIR319a microRNA locus in Arabidopsis and related Brassicaceae.
    Mol Biol Evol. 2008 May;25(5):892-902 PMID: 18296705
  19. Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance.
    Nat Biotechnol. 2006 Nov;24(11):1420-8 PMID: 17057702
  20. Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species.
    Plant Cell. 2006 May;18(5):1134-51 PMID: 16603651
  21. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues.
    EMBO J. 1999 Apr 15;18(8):2066-73 PMID: 10205161
  22. The Arabidopsis Phosphatidylinositol Phosphate 5-Kinase PIP5K3 is a key regulator of root hair tip growth.
    Plant Cell. 2008 Feb;20(2):367-80 PMID: 18281506
  23. Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants.
    Plant J. 2000 Oct;24(2):265-73 PMID: 11069700
  24. AXR4 is required for localization of the auxin influx facilitator AUX1.
    Science. 2006 May 26;312(5777):1218-20 PMID: 16690816
  25. The Vac14p-Fig4p complex acts independently of Vac7p and couples PI3,5P2 synthesis and turnover.
    J Cell Biol. 2006 Feb 27;172(5):693-704 PMID: 16492811
  26. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation.
    J Biosci Bioeng. 2007 Jul;104(1):34-41 PMID: 17697981
  27. Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation.
    Development. 2004 Apr;131(7):1491-501 PMID: 14985254
  28. Subcellular trafficking of PIN auxin efflux carriers in auxin transport.
    Eur J Cell Biol. 2010 Feb-Mar;89(2-3):231-5 PMID: 19944476
  29. PtdIns(3,5)P2 is required for delivery of endocytic cargo into the multivesicular body.
    Traffic. 2003 Jul;4(7):479-90 PMID: 12795693
  30. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body.
    Cell. 1998 Dec 11;95(6):847-58 PMID: 9865702
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2011-02-00
Epub
2010-00-20
Pages
797-807
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3032467
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: product@genelibs.com