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PMID: 18583529 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis.

Plant physiology ·Vol. 147 ·No. 4 ·2008-08-00 ·Pages 1690-8

Monshausen GB, Messerli MA, Gilroy S

Abstract

In tip-growing cells, the tip-high Ca(2+) gradient is thought to regulate the activity of components of the growth machinery, including the cytoskeleton, Ca(2+)-dependent regulatory proteins, and the secretory apparatus. In pollen tubes, both the Ca(2+) gradient and cell elongation show oscillatory behavior, reinforcing the link between the two. We report that in growing root hairs of Arabidopsis (Arabidopsis thaliana), an oscillating tip-focused Ca(2+) gradient can be resolved through imaging of a cytosolically expressed Yellow Cameleon 3.6 fluorescence resonance energy transfer-based Ca(2+) sensor. Both elongation of the root hairs and the associated tip-focused Ca(2+) gradient show a similar dynamic character, oscillating with a frequency of 2 to 4 min(-1). Cross-correlation analysis indicates that the Ca(2+) oscillations lag the growth oscillations by 5.3 +/- 0.3 s. However, growth never completely stops, even during the slow cycle of an oscillation, and the concomitant tip Ca(2+) level is always slightly elevated compared with the resting Ca(2+) concentration along the distal shaft, behind the growing tip. Artificially increasing Ca(2+) using the Ca(2+) ionophore A23187 leads to immediate cessation of elongation and thickening of the apical cell wall. In contrast, dissipating the Ca(2+) gradient using either the Ca(2+) channel blocker La(3+) or the Ca(2+) chelator EGTA is accompanied by an increase in the rate of cell expansion and eventual bursting of the root hair tip. These observations are consistent with a model in which the maximal oscillatory increase in cytosolic Ca(2+) is triggered by cell expansion associated with tip growth and plays a role in the subsequent restriction of growth.

MeSH Terms
Arabidopsis/cytology,drug effects,metabolism Calcimycin/pharmacology Calcium/metabolism Cell Enlargement/drug effects Cytosol/metabolism Fluorescence Resonance Energy Transfer Ionophores/pharmacology Kinetics Luminescent Proteins/analysis Plant Roots/cytology,drug effects,metabolism Recombinant Proteins/analysis
Chemicals
Ionophores Luminescent Proteins Recombinant Proteins Calcimycin Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Monshausen Gabriele B
Department of Botany, University of Wisconsin, Madison, Wisconsin 53706, USA.
Messerli Mark A
Gilroy Simon
References (40)
40 references, click to expand
  1. Differential activation of transcription factors induced by Ca2+ response amplitude and duration.
    Nature. 1997 Apr 24;386(6627):855-8 PMID: 9126747
  2. Identification and characterization of a Ca2+-dependent actin filament-severing protein from lily pollen.
    Plant Physiol. 2004 Dec;136(4):3979-89 PMID: 15557101
  3. Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10554-9 PMID: 15247428
  4. Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by a calcium-stimulated protein kinase and is essential for the control of functional activity.
    Plant J. 1998 Apr;14(2):187-93 PMID: 9669865
  5. Phosphorylation of plant actin-depolymerising factor by calmodulin-like domain protein kinase.
    FEBS Lett. 2001 Jun 15;499(1-2):97-100 PMID: 11418120
  6. Gateway-compatible vectors for plant functional genomics and proteomics.
    Plant J. 2006 Feb;45(4):616-29 PMID: 16441352
  7. Spatial Organization of Calcium Signaling Involved in Cell Volume Control in the Fucus Rhizoid.
    Plant Cell. 1996 Nov;8(11):2015-2031 PMID: 12239374
  8. Pulsatile influxes of H+, K+ and Ca2+ lag growth pulses of Lilium longiflorum pollen tubes.
    J Cell Sci. 1999 May;112 ( Pt 10):1497-509 PMID: 10212144
  9. The role of plant villin in the organization of the actin cytoskeleton, cytoplasmic streaming and the architecture of the transvacuolar strand in root hair cells of Hydrocharis.
    Planta. 2000 Apr;210(5):836-43 PMID: 10805457
  10. A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana.
    J Cell Biol. 2006 Mar 27;172(7):991-8 PMID: 16567499
  11. Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum.
    J Cell Sci. 1997 Jun;110 ( Pt 11):1269-78 PMID: 9202387
  12. Cellular oscillations and the regulation of growth: the pollen tube paradigm.
    Bioessays. 2001 Jan;23(1):86-94 PMID: 11135313
  13. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  14. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs.
    Proc Natl Acad Sci U S A. 2007 Dec 26;104(52):20996-1001 PMID: 18079291
  15. Purification and immunolocalization of an annexin-like protein in pea seedlings.
    Planta. 1992;187:1-9 PMID: 11538119
  16. Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models.
    Planta. 2003 May;217(1):147-57 PMID: 12721859
  17. Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs.
    Plant Cell. 2003 Jan;15(1):285-92 PMID: 12509537
  18. Tip-localized calcium entry fluctuates during pollen tube growth.
    Dev Biol. 1996 Feb 25;174(1):160-73 PMID: 8626016
  19. Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity.
    Plant Cell. 2006 Apr;18(4):867-78 PMID: 16531501
  20. Properties and partial protein sequence of plant annexins.
    Plant Physiol. 1992 Jul;99(3):864-71 PMID: 16669013
  21. Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth.
    Dev Biol. 2000 Jun 1;222(1):84-98 PMID: 10885748
  22. The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells.
    Plant Cell. 2004 Jun;16(6):1589-603 PMID: 15155878
  23. Plant villin, lily P-135-ABP, possesses G-actin binding activity and accelerates the polymerization and depolymerization of actin in a Ca2+-sensitive manner.
    Plant Cell Physiol. 2005 Oct;46(10):1690-703 PMID: 16100394
  24. Localized Apical Increases of Cytosolic Free Calcium Control Pollen Tube Orientation.
    Plant Cell. 1996 Nov;8(11):1935-1949 PMID: 12239370
  25. Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplasts
    Plant Cell. 1998 Aug;10(8):1267-76 PMID: 9707528
  26. Correlative Analysis of [Ca](C) and Apical Secretion during Pollen Tube Growth and Reorientation.
    Plant Signal Behav. 2006 May;1(3):152-7 PMID: 19521495
  27. Through form to function: root hair development and nutrient uptake.
    Trends Plant Sci. 2000 Feb;5(2):56-60 PMID: 10664614
  28. Identification and characterization of stretch-activated ion channels in pollen protoplasts.
    Plant Physiol. 2004 Jul;135(3):1398-406 PMID: 15247410
  29. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana.
    Plant J. 1997 Aug;12(2):427-39 PMID: 9301093
  30. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin.
    Nature. 1997 Aug 28;388(6645):882-7 PMID: 9278050
  31. Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments.
    Plant Physiol. 2004 Dec;136(4):3892-904 PMID: 15542492
  32. Pollen Tube Growth and the Intracellular Cytosolic Calcium Gradient Oscillate in Phase while Extracellular Calcium Influx Is Delayed.
    Plant Cell. 1997 Nov;9(11):1999-2010 PMID: 12237353
  33. Time series analysis demonstrates the absence of pulsatile hyphal growth.
    Microbiology (Reading). 2003 Nov;149(Pt 11):3111-3119 PMID: 14600223
  34. Calcium ionophore A 23187 affects localized wall secretion in the tip region of pollen tubes of Lilium longiflorum.
    Planta. 1979 Jan;145(3):225-32 PMID: 24317727
  35. Relocation of a Ca2+-dependent protein kinase activity during pollen tube reorientation
    Plant Cell. 1998 Sep;10(9):1499-510 PMID: 9724696
  36. Pulsed growth of fungal hyphal tips.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12228-32 PMID: 7991610
  37. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.
    Nature. 2003 Mar 27;422(6930):442-6 PMID: 12660786
  38. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes.
    Mol Biol Cell. 2005 Nov;16(11):5385-99 PMID: 16148045
  39. Local positive feedback regulation determines cell shape in root hair cells.
    Science. 2008 Feb 29;319(5867):1241-4 PMID: 18309082
  40. Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity.
    Planta. 1997 Dec;203(4):495-505 PMID: 9421933
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2008-08-00
Epub
2008-00-26
Pages
1690-8
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2492656
Subset
IM
Grants
PHS HHS · NCRR P41 RR-001395 · United States
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