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PMID: 25591940 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The Arabidopsis alkaline ceramidase TOD1 is a key turgor pressure regulator in plant cells.

Nature communications ·Vol. 6 ·2015-01-16 ·Pages 6030

Chen LY, Shi DQ, Zhang WJ, Tang ZS, Liu J, Yang WC

Abstract

Turgor pressure plays pivotal roles in the growth and movement of walled cells that make up plants and fungi. However, the molecular mechanisms regulating turgor pressure and the coordination between turgor pressure and cell wall remodelling for cell growth remain poorly understood. Here, we report the characterization of Arabidopsis TurgOr regulation Defect 1 (TOD1), which is preferentially expressed in pollen tubes and silique guard cells. We demonstrate that TOD1 is a Golgi-localized alkaline ceramidase. tod1 mutant pollen tubes have higher turgor than wild type and show growth retardation both in pistils and in agarose medium. In addition, tod1 guard cells are insensitive to abscisic acid (ABA)-induced stomatal closure, whereas sphingosine-1-phosphate, a putative downstream component of ABA signalling and product of alkaline ceramidases, promotes closure in both wild type and tod1. Our data suggest that TOD1 acts in turgor pressure regulation in both guard cells and pollen tubes.

MeSH Terms
Alkaline Ceramidase/metabolism Arabidopsis/enzymology,metabolism Arabidopsis Proteins/metabolism Lysophospholipids/metabolism Plant Stomata/metabolism Pollen Tube/enzymology,metabolism Signal Transduction Sphingosine/analogs & derivatives,metabolism
Chemicals
Arabidopsis Proteins Lysophospholipids sphingosine 1-phosphate Alkaline Ceramidase Sphingosine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Chen Li-Yu
1] State Key Laboratory of Molecular Developmental Biology and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China [2] University of Chinese Academy of Sciences, Beijing 100049, China.
Shi Dong-Qiao
State Key Laboratory of Molecular Developmental Biology and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Zhang Wen-Juan
1] State Key Laboratory of Molecular Developmental Biology and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China [2] University of Chinese Academy of Sciences, Beijing 100049, China.
Tang Zuo-Shun
State Key Laboratory of Molecular Developmental Biology and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Liu Jie
State Key Laboratory of Molecular Developmental Biology and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Yang Wei-Cai
1] State Key Laboratory of Molecular Developmental Biology and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China [2] Collaborative Innovation Center for Genetics and Development, Fudan University, Shanghai 200433, China.
References (63)
63 references, click to expand
  1. Isolation and expression of an anther-specific gene from tomato.
    Mol Gen Genet. 1989 Jun;217(2-3):240-5 PMID: 2770694
  2. Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide.
    J Biol Chem. 2000 Oct 6;275(40):31369-78 PMID: 10900202
  3. Double fertilization - caught in the act.
    Trends Plant Sci. 2008 Aug;13(8):437-43 PMID: 18650119
  4. Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth.
    PLoS One. 2011;6(4):e18549 PMID: 21541026
  5. Under pressure, cell walls set the pace.
    Trends Plant Sci. 2010 Jul;15(7):363-9 PMID: 20483654
  6. Functional characterization of a higher plant sphingolipid Delta4-desaturase: defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis.
    Plant Physiol. 2009 Jan;149(1):487-98 PMID: 18978071
  7. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  8. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes.
    Plant J. 2004 Sep;39(5):761-75 PMID: 15315637
  9. Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth.
    Planta. 2006 Mar;223(4):736-45 PMID: 16208487
  10. Transient expression and analysis of fluorescent reporter proteins in plant pollen tubes.
    Nat Protoc. 2011 Apr;6(4):419-26 PMID: 21412270
  11. Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity.
    J Biol Chem. 2000 Mar 10;275(10):6876-84 PMID: 10702247
  12. Cloning and characterization of a novel human alkaline ceramidase. A mammalian enzyme that hydrolyzes phytoceramide.
    J Biol Chem. 2001 Jul 13;276(28):26577-88 PMID: 11356846
  13. Alkaline ceramidase 2 (ACER2) and its product dihydrosphingosine mediate the cytotoxicity of N-(4-hydroxyphenyl)retinamide in tumor cells.
    J Biol Chem. 2010 Sep 17;285(38):29078-90 PMID: 20628055
  14. Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry.
    Rapid Commun Mass Spectrom. 2007;21(7):1304-14 PMID: 17340572
  15. Identification of a novel amidase motif in neutral ceramidase.
    Biochem J. 2006 Feb 1;393(Pt 3):687-95 PMID: 16229686
  16. Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense.
    Planta. 2005 Feb;220(4):582-92 PMID: 15449057
  17. POLLEN GERMINATION AND TUBE GROWTH.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:461-491 PMID: 15012271
  18. Four Na+/H+ exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation.
    J Biol Chem. 2005 Jan 14;280(2):1561-72 PMID: 15522866
  19. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  20. NPS@: network protein sequence analysis.
    Trends Biochem Sci. 2000 Mar;25(3):147-50 PMID: 10694887
  21. The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana.
    Curr Biol. 2007 Jul 3;17(13):1101-8 PMID: 17600712
  22. Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil.
    PLoS Genet. 2009 Aug;5(8):e1000621 PMID: 19714218
  23. Understanding pollen tube growth: the hydrodynamic model versus the cell wall model.
    Trends Plant Sci. 2011 Jul;16(7):347-52 PMID: 21514877
  24. Periplasm turgor pressure controls wall deposition and assembly in growing Chara corallina cells.
    Ann Bot. 2006 Jul;98(1):93-105 PMID: 16720633
  25. The emerging role of forces in axonal elongation.
    Prog Neurobiol. 2011 Jul;94(2):91-101 PMID: 21527310
  26. Cloning and characterization of a mouse endoplasmic reticulum alkaline ceramidase: an enzyme that preferentially regulates metabolism of very long chain ceramides.
    J Biol Chem. 2003 Aug 15;278(33):31184-91 PMID: 12783875
  27. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR.
    Plant J. 1995 Sep;8(3):457-63 PMID: 7550382
  28. Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins.
    Nature. 2003 Jun 5;423(6940):651-4 PMID: 12789341
  29. Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases.
    J Biol Chem. 2011 Apr 15;286(15):13336-45 PMID: 21330371
  30. Pollen tubes and the physical world.
    Trends Plant Sci. 2011 Jul;16(7):353-5 PMID: 21536475
  31. Molecular cloning and characterization of OsCDase, a ceramidase enzyme from rice.
    Plant J. 2008 Sep;55(6):1000-9 PMID: 18547394
  32. Cytochemical Analysis of Pollen Development in Wild-Type Arabidopsis and a Male-Sterile Mutant.
    Plant Cell. 1990 Sep;2(9):877-889 PMID: 12354970
  33. Sub-piconewton force fluctuations of actomyosin in vitro.
    Nature. 1991 Jul 25;352(6333):301-6 PMID: 1830130
  34. The art and design of genetic screens: Arabidopsis thaliana.
    Nat Rev Genet. 2002 Feb;3(2):124-36 PMID: 11836506
  35. Life under pressure: hydrostatic pressure in cell growth and function.
    Trends Plant Sci. 2007 Mar;12(3):90-7 PMID: 17293155
  36. Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties.
    Dev Biol. 2009 Oct 15;334(2):437-46 PMID: 19666018
  37. Stomata: key players in the earth system, past and present.
    Curr Opin Plant Biol. 2010 Jun;13(3):233-40 PMID: 20552724
  38. Delayed activation of the paternal genome during seed development.
    Nature. 2000 Mar 2;404(6773):91-4 PMID: 10716449
  39. Phosphorylation of sphingoid long-chain bases in Arabidopsis: functional characterization and expression of the first sphingoid long-chain base Kinase gene in plants.
    Plant Cell Physiol. 2005 Feb;46(2):375-80 PMID: 15695468
  40. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues.
    Plant Mol Biol. 1985 Mar;5(2):69-76 PMID: 24306565
  41. Arabidopsis galacturonosyltransferase (GAUT) 13 and GAUT14 have redundant functions in pollen tube growth.
    Mol Plant. 2013 Jul;6(4):1131-48 PMID: 23709340
  42. The 3,000 rice genomes project.
    Gigascience. 2014 May 28;3:7 PMID: 24872877
  43. Golgi alkaline ceramidase regulates cell proliferation and survival by controlling levels of sphingosine and S1P.
    FASEB J. 2006 Sep;20(11):1813-25 PMID: 16940153
  44. Involvement of sphingosine kinase in plant cell signalling.
    Plant J. 2008 Oct;56(1):64-72 PMID: 18557834
  45. Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth.
    Plant Physiol. 2009 Jul;150(3):1322-34 PMID: 19474213
  46. A versatile stain for pollen fungi, yeast and bacteria.
    Stain Technol. 1980 Jan;55(1):13-8 PMID: 6158141
  47. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate.
    Nature. 2001 Mar 29;410(6828):596-9 PMID: 11279499
  48. Organelle pH studies using targeted avidin and fluorescein-biotin.
    Chem Biol. 2000 Mar;7(3):197-209 PMID: 10712929
  49. Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana.
    Plant J. 2007 Nov;52(3):570-82 PMID: 17764500
  50. The PANTHER database of protein families, subfamilies, functions and pathways.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D284-8 PMID: 15608197
  51. Genome sequencing reveals agronomically important loci in rice using MutMap.
    Nat Biotechnol. 2012 Feb;30(2):174-8 PMID: 22267009
  52. Fast and accurate short read alignment with Burrows-Wheeler transform.
    Bioinformatics. 2009 Jul 15;25(14):1754-60 PMID: 19451168
  53. Diverse cell signalling pathways regulate pollen-stigma interactions: the search for consensus.
    New Phytol. 2008 Jul;179(2):286-317 PMID: 19086285
  54. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
    Mol Biol Evol. 2007 Aug;24(8):1596-9 PMID: 17488738
  55. PANTHER: a library of protein families and subfamilies indexed by function.
    Genome Res. 2003 Sep;13(9):2129-41 PMID: 12952881
  56. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements.
    Genes Dev. 1995 Jul 15;9(14):1797-810 PMID: 7622040
  57. Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method.
    Nat Protoc. 2007;2(1):35-7 PMID: 17401335
  58. Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth.
    Plant Cell. 2002 Apr;14(4):945-62 PMID: 11971147
  59. Upregulation of the human alkaline ceramidase 1 and acid ceramidase mediates calcium-induced differentiation of epidermal keratinocytes.
    J Invest Dermatol. 2008 Feb;128(2):389-97 PMID: 17713573
  60. Principles of bioactive lipid signalling: lessons from sphingolipids.
    Nat Rev Mol Cell Biol. 2008 Feb;9(2):139-50 PMID: 18216770
  61. How does a hypha grow? The biophysics of pressurized growth in fungi.
    Nat Rev Microbiol. 2011 Jul;9(7):509-18 PMID: 21643041
  62. The mechanisms of pollination and fertilization in plants.
    Annu Rev Cell Dev Biol. 2002;18:81-105 PMID: 12142268
  63. Biomechanics of plant growth.
    Am J Bot. 2006 Oct;93(10):1415-25 PMID: 21642088
Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
Published
2015-01-16
Epub
2015-00-16
Pages
6030
Language
English
Region
England
NLM ID
101528555
PMCID
PMC4309442
Subset
IM
Databases
Analysis Services
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