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PMID: 19861555 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes.

The Plant cell ·Vol. 21 ·No. 10 ·2009-10-00 ·Pages 3026-40

McKenna ST, Kunkel JG, Bosch M, Rounds CM, Vidali L, Winship LJ, Hepler PK

Abstract

We examined exocytosis during oscillatory growth in lily (Lilium formosanum and Lilium longiflorum) and tobacco (Nicotiana tabacum) pollen tubes using three markers: (1) changes in cell wall thickness by Nomarski differential interference contrast (DIC), (2) changes in apical cell wall fluorescence in cells stained with propidium iodide (PI), and (3) changes in apical wall fluorescence in cells expressing tobacco pectin methyl esterase fused to green fluorescent protein (PME-GFP). Using PI fluorescence, we quantified oscillatory changes in the amount of wall material from both lily and tobacco pollen tubes. Measurement of wall thickness by DIC was only possible with lily due to limitations of microscope resolution. PME-GFP, a direct marker for exocytosis, only provides information in tobacco because its expression in lily causes growth inhibition and cell death. We show that exocytosis in pollen tubes oscillates and leads the increase in growth rate; the mean phase difference between exocytosis and growth is -98 degrees +/- 3 degrees in lily and -124 degrees +/- 4 degrees in tobacco. Statistical analyses reveal that the anticipatory increase in wall material predicts, to a high degree, the rate and extent of the subsequent growth surge. Exocytosis emerges as a prime candidate for the initiation and regulation of oscillatory pollen tube growth.

MeSH Terms
Carboxylic Ester Hydrolases/genetics,metabolism Cell Wall/metabolism Exocytosis/genetics,physiology Green Fluorescent Proteins/genetics,metabolism Lilium/genetics,growth & development,metabolism Molecular Sequence Data Pollen Tube/genetics,growth & development,metabolism Tobacco/genetics,growth & development,metabolism
Chemicals
Green Fluorescent Proteins Carboxylic Ester Hydrolases pectinesterase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
McKenna Sylvester T
Department of Biology, Long Island University, Brooklyn, New York 11201, USA.
Kunkel Joseph G
Bosch Maurice
Rounds Caleb M
Vidali Luis
Winship Lawrence J
Hepler Peter K
References (59)
59 references, click to expand
  1. Detection and localization of pectin methylesterase isoforms in pollen tubes of Nicotiana tabacum L.
    Planta. 2002 Mar;214(5):734-40 PMID: 11882942
  2. Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes.
    J Exp Bot. 2008;59(4):861-73 PMID: 18304978
  3. Molecular Mechanisms of Pollen Tube Growth and Differentiation.
    Plant Cell. 1993 Oct;5(10):1303-1314 PMID: 12271030
  4. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth.
    Science. 2001 Oct 26;294(5543):846-9 PMID: 11679668
  5. Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization.
    Plant Physiol. 2008 Apr;146(4):1611-21 PMID: 18263780
  6. Cellular oscillations and the regulation of growth: the pollen tube paradigm.
    Bioessays. 2001 Jan;23(1):86-94 PMID: 11135313
  7. Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily.
    Plant Cell. 2006 Sep;18(9):2182-93 PMID: 16920777
  8. Structural and signaling networks for the polar cell growth machinery in pollen tubes.
    Annu Rev Plant Biol. 2008;59:547-72 PMID: 18444907
  9. Electrostatic effects and the dynamics of enzyme reactions at the surface of plant cells. 2. The role of pectin methyl esterase in the modulation of electrostatic effects in soybean cell walls.
    Eur J Biochem. 1986 Feb 17;155(1):191-7 PMID: 3948878
  10. Dynamic continuity of cytoplasmic and membrane compartments between plant cells.
    J Cell Biol. 1988 Mar;106(3):715-21 PMID: 3346323
  11. A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes.
    Dev Biol. 1991 Dec;148(2):612-9 PMID: 1743404
  12. Investigation of the action patterns of pectinmethylesterase isoforms through kinetic analyses and NMR spectroscopy. Implications In cell wall expansion.
    J Biol Chem. 1998 Dec 11;273(50):33150-6 PMID: 9837882
  13. Polarized growth: maintaining focus on the tip.
    Curr Opin Plant Biol. 2006 Dec;9(6):579-88 PMID: 17010659
  14. The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana.
    Plant Cell. 2009 Feb;21(2):526-44 PMID: 19208902
  15. Tip-localized calcium entry fluctuates during pollen tube growth.
    Dev Biol. 1996 Feb 25;174(1):160-73 PMID: 8626016
  16. 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
  17. Pectin: cell biology and prospects for functional analysis.
    Plant Mol Biol. 2001 Sep;47(1-2):9-27 PMID: 11554482
  18. Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth.
    J Cell Biol. 2008 Jun 30;181(7):1155-68 PMID: 18591430
  19. New ways to look at the architecture of plant cell walls : localization of polygalacturonate blocks in plant tissues.
    Plant Physiol. 1989 Sep;91(1):31-3 PMID: 16667016
  20. Exocytosis and endocytosis
    Plant Cell. 1999 Apr;11(4):643-60 PMID: 10213784
  21. Endo/exocytosis in the pollen tube apex is differentially regulated by Ca2+ and GTPases.
    J Exp Bot. 2003 Jan;54(380):83-92 PMID: 12456758
  22. How pollen tubes grow.
    Dev Biol. 2007 Mar 15;303(2):405-20 PMID: 17214979
  23. Pectin methylesterases and pectin dynamics in pollen tubes.
    Plant Cell. 2005 Dec;17(12):3219-26 PMID: 16322606
  24. Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching.
    Plant Physiol. 2008 Aug;147(4):1646-58 PMID: 18508956
  25. Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion.
    Plant Cell. 2008 Dec;20(12):3312-30 PMID: 19060112
  26. Mobile factories: Golgi dynamics in plant cells.
    Trends Plant Sci. 2001 Apr;6(4):160-7 PMID: 11286921
  27. Periplasm turgor pressure controls wall deposition and assembly in growing Chara corallina cells.
    Ann Bot. 2006 Jul;98(1):93-105 PMID: 16720633
  28. Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes.
    J Cell Sci. 2001 Jul;114(Pt 14):2685-95 PMID: 11683395
  29. Differential organelle movement on the actin cytoskeleton in lily pollen tubes.
    Cell Motil Cytoskeleton. 2007 Mar;64(3):217-32 PMID: 17245769
  30. Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis
    Plant J. 1999 Aug;19(4):379-86 PMID: 10504560
  31. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide.
    Annu Rev Plant Biol. 2004;55:109-39 PMID: 15377216
  32. Membrane trafficking and polar growth in root hairs and pollen tubes.
    J Exp Bot. 2007;58(1):65-74 PMID: 16873451
  33. Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube.
    Planta. 2005 Apr;221(1):95-104 PMID: 15747143
  34. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes.
    J Cell Biol. 2001 Mar 5;152(5):1019-32 PMID: 11238457
  35. Pectin methylesterase, a regulator of pollen tube growth.
    Plant Physiol. 2005 Jul;138(3):1334-46 PMID: 15951488
  36. NAD(P)H oscillates in pollen tubes and is correlated with tip growth.
    Plant Physiol. 2006 Dec;142(4):1460-8 PMID: 17041030
  37. Rates of exocytosis and endocytosis in Arabidopsis root hairs and pollen tubes.
    J Microsc. 2008 Aug;231(2):265-73 PMID: 18778424
  38. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media.
    Plant Cell. 1994 Dec;6(12):1815-28 PMID: 7866026
  39. Cell surface expansion in polarly growing root hairs of Medicago truncatula.
    Plant Physiol. 2000 Nov;124(3):959-70 PMID: 11080274
  40. Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco.
    Plant Cell. 2005 Sep;17(9):2564-79 PMID: 16100336
  41. Uncovering hidden treasures in pollen tube growth mechanics.
    Trends Plant Sci. 2009 Jun;14(6):318-27 PMID: 19446491
  42. 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
  43. Ca(2)+-stimulated exocytosis in maize coleoptile cells.
    Plant Cell. 2000 Jul;12(7):1127-36 PMID: 10899979
  44. Identifying cytoplasmic input to the cell wall of growing Chara corallina.
    J Exp Bot. 2006;57(12):3231-42 PMID: 16893975
  45. Ca2+-independent and Ca2+/GTP-binding protein-controlled exocytosis in a plant cell.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6565-70 PMID: 11038550
  46. Membrane recycling and the control of secretory activity in pollen tubes.
    J Cell Sci. 1983 Sep;63:303-10 PMID: 6630312
  47. Microfluorometry of pectic materials in the dehiscence zone of almond (Prunus dulcis [Mill.] DA Webb) fruits.
    J Histochem Cytochem. 1988 Aug;36(8):1037-41 PMID: 3392393
  48. CELL WALL CARBOHYDRATE EPITOPES IN THE GREEN ALGA OEDOGONIUM BHARUCHAE F. MINOR (OEDOGONIALES, CHLOROPHYTA)(1).
    J Phycol. 2008 Oct;44(5):1257-68 PMID: 27041722
  49. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway.
    Plant Cell. 2005 Sep;17(9):2542-53 PMID: 16055633
  50. Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes.
    Plant Cell. 2008 Mar;20(3):614-34 PMID: 18364468
  51. Calcium pectate chemistry controls growth rate of Chara corallina.
    J Exp Bot. 2006;57(15):3989-4002 PMID: 17110588
  52. Turgor pressure moves polysaccharides into growing cell walls of Chara corallina.
    Ann Bot. 2005 May;95(6):967-79 PMID: 15760911
  53. Pollen-specific pectin methylesterase involved in pollen tube growth.
    Dev Biol. 2006 Jun 1;294(1):83-91 PMID: 16564517
  54. Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold.
    J Cell Sci. 2007 Nov 1;120(Pt 21):3804-19 PMID: 17940063
  55. The plant cell wall polysaccharide rhamnogalacturonan II self-assembles into a covalently cross-linked dimer.
    J Biol Chem. 1999 May 7;274(19):13098-104 PMID: 10224062
  56. The mechanics of surface expansion anisotropy in Medicago truncatula root hairs.
    Plant Physiol. 2004 Oct;136(2):3266-75 PMID: 15448192
  57. The Pore Size of Non-Graminaceous Plant Cell Walls Is Rapidly Decreased by Borate Ester Cross-Linking of the Pectic Polysaccharide Rhamnogalacturonan II.
    Plant Physiol. 1999 Nov;121(3):829-838 PMID: 10557231
  58. The catalytic site of the pectin biosynthetic enzyme alpha-1,4-galacturonosyltransferase is located in the lumen of the Golgi.
    Plant Physiol. 2001 Sep;127(1):360-71 PMID: 11553763
  59. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes.
    Mol Biol Cell. 2005 Nov;16(11):5385-99 PMID: 16148045
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2009-10-00
Epub
2009-00-27
Pages
3026-40
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2782290
Subset
IM
Databases
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