Home LiteratureArticle Details
PMID: 12417710 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Regulation of the pollen-specific actin-depolymerizing factor LlADF1.

The Plant cell ·Vol. 14 ·No. 11 ·2002-11-00 ·Pages 2915-27

Allwood EG, Anthony RG, Smertenko AP, Reichelt S, Drobak BK, Doonan JH, Weeds AG, Hussey PJ

Abstract

Pollen tube growth is dependent on a dynamic actin cytoskeleton, suggesting that actin-regulating proteins are involved. We have examined the regulation of the lily pollen-specific actin-depolymerizing factor (ADF) LlADF1. Its actin binding and depolymerizing activity is pH sensitive, inhibited by certain phosphoinositides, but not controlled by phosphorylation. Compared with its F-actin binding properties, its low activity in depolymerization assays has been used to explain why pollen ADF decorates F-actin in pollen grains. This low activity is incompatible with a role in increasing actin dynamics necessary to promote pollen tube growth. We have identified a plant homolog of actin-interacting protein, AIP1, which enhances the depolymerization of F-actin in the presence of LlADF1 by approximately 60%. Both pollen ADF and pollen AIP1 bind F-actin in pollen grains but are mainly cytoplasmic in pollen tubes. Our results suggest that together these proteins remodel actin filaments as pollen grains enter and exit dormancy.

MeSH Terms
Actin Depolymerizing Factors Actins/metabolism Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Brassica napus/genetics,metabolism Carrier Proteins/genetics,metabolism Cloning, Molecular Conserved Sequence/genetics Cytoskeleton/metabolism Destrin Gene Expression Regulation, Plant/genetics Hydrogen-Ion Concentration Lilium/genetics,metabolism Magnoliopsida/genetics,metabolism Microfilament Proteins/drug effects,genetics,metabolism Phospholipids/pharmacology Phosphorylation Phylogeny Plant Proteins/genetics,metabolism Pollen/genetics,growth & development,metabolism Saccharomyces cerevisiae/genetics,metabolism Two-Hybrid System Techniques Zea mays/genetics,metabolism
Chemicals
AIP1 protein, Arabidopsis Actin Depolymerizing Factors Actins Arabidopsis Proteins Carrier Proteins Destrin Microfilament Proteins Phospholipids Plant Proteins actin interacting protein 1
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Allwood Ellen G
Integrative Cell Biology Laboratory, School of Biological and Biomedical Sciences, University of Durham, South Road, Durham DH1 3LE, United Kingdom.
Anthony Richard G
Smertenko Andrei P
Reichelt Stefanie
Drobak Bjorn K
Doonan John H
Weeds Alan G
Hussey Patrick J
References (52)
52 references, click to expand
  1. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3.
    Curr Biol. 2000 Mar 23;10(6):311-20 PMID: 10744973
  2. Two closely related cDNAs encoding actin-depolymerizing factors of petunia are mainly expressed in vegetative tissues.
    Gene. 2000 Oct 31;257(2):167-76 PMID: 11080583
  3. Interaction of pollen-specific actin-depolymerizing factor with actin.
    Plant J. 2001 Jan;25(2):203-12 PMID: 11169196
  4. 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
  5. The Caenorhabditis elegans unc-78 gene encodes a homologue of actin-interacting protein 1 required for organized assembly of muscle actin filaments.
    J Cell Biol. 2001 Mar 19;152(6):1313-9 PMID: 11257131
  6. Cofilin phosphorylation by protein kinase testicular protein kinase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation.
    Mol Biol Cell. 2001 Apr;12(4):1131-45 PMID: 11294912
  7. ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis.
    Plant Cell. 2001 Jun;13(6):1333-46 PMID: 11402164
  8. Molecular identification and characterization of the Arabidopsis AtADF1, AtADFS and AtADF6 genes.
    Plant Mol Biol. 2001 Mar;45(5):517-27 PMID: 11414611
  9. Phosphorylation of plant actin-depolymerising factor by calmodulin-like domain protein kinase.
    FEBS Lett. 2001 Jun 15;499(1-2):97-100 PMID: 11418120
  10. Interaction of elongation factor 1alpha from Zea mays (ZmEF-1alpha) with F-actin and interplay with the maize actin severing protein, ZmADF3.
    Cell Motil Cytoskeleton. 2001 Jun;49(2):104-11 PMID: 11443740
  11. A protein interaction map for cell polarity development.
    J Cell Biol. 2001 Aug 6;154(3):549-71 PMID: 11489916
  12. Cofilin phosphorylation and actin reorganization activities of testicular protein kinase 2 and its predominant expression in testicular Sertoli cells.
    J Biol Chem. 2001 Aug 17;276(33):31449-58 PMID: 11418599
  13. cAMP acts as a second messenger in pollen tube growth and reorientation.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10481-6 PMID: 11517303
  14. Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane.
    Biochim Biophys Acta. 2001 Oct 31;1533(3):190-206 PMID: 11731330
  15. Determining the differences in actin binding by human ADF and cofilin.
    J Mol Biol. 2002 Jan 25;315(4):911-25 PMID: 11812157
  16. The ADF/cofilin family: actin-remodeling proteins.
    Genome Biol. 2002;3(5):reviews3007 PMID: 12049672
  17. An actin-depolymerizing protein (depactin) from starfish oocytes: properties and interaction with actin.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1612-21 PMID: 6226671
  18. pH control of actin polymerization by cofilin.
    J Biol Chem. 1985 Nov 25;260(27):14410-2 PMID: 4055781
  19. Differential and developmental expression of beta-tubulins in a higher plant.
    J Biol Chem. 1988 Apr 15;263(11):5474-9 PMID: 3281942
  20. Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with actin by phosphoinositides.
    J Biol Chem. 1990 May 25;265(15):8382-6 PMID: 2160454
  21. A short sequence responsible for both phosphoinositide binding and actin binding activities of cofilin.
    J Biol Chem. 1991 Sep 15;266(26):17218-21 PMID: 1654325
  22. The actin filament severing protein actophorin promotes the formation of rigid bundles of actin filaments crosslinked with alpha-actinin.
    J Cell Biol. 1991 Dec;115(6):1621-8 PMID: 1757466
  23. LEAFY controls floral meristem identity in Arabidopsis.
    Cell. 1992 May 29;69(5):843-59 PMID: 1350515
  24. Molecular cloning and characterization of anther-preferential cDNA encoding a putative actin-depolymerizing factor.
    Plant Mol Biol. 1993 Jan;21(1):39-45 PMID: 8425049
  25. Primary structure of and studies on Acanthamoeba actophorin.
    Biochemistry. 1993 Aug 24;32(33):8525-33 PMID: 8357799
  26. Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments.
    Biochemistry. 1993 Sep 28;32(38):9985-93 PMID: 8399167
  27. Analysis of the interactions of actin depolymerizing factor with G- and F-actin.
    Biochemistry. 1993 Sep 28;32(38):9994-10004 PMID: 8399168
  28. Actophorin preferentially binds monomeric ADP-actin over ATP-bound actin: consequences for cell locomotion.
    FEBS Lett. 1994 Jun 27;347(2-3):251-6 PMID: 8034013
  29. The ancient regulatory-protein family of WD-repeat proteins.
    Nature. 1994 Sep 22;371(6495):297-300 PMID: 8090199
  30. A Zea mays pollen cDNA encoding a putative actin-depolymerizing factor.
    Plant Physiol. 1995 Mar;107(3):1011-2 PMID: 7716228
  31. Defining protein interactions with yeast actin in vivo.
    Nat Struct Biol. 1995 Jan;2(1):28-35 PMID: 7719850
  32. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin.
    Cell. 1995 Apr 7;81(1):41-51 PMID: 7720072
  33. The Arabidopsis profilin gene family. Evidence for an ancient split between constitutive and pollen-specific profilin genes.
    Plant Physiol. 1996 May;111(1):115-26 PMID: 8685262
  34. Pollen specific expression of maize genes encoding actin depolymerizing factor-like proteins.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7415-20 PMID: 8693008
  35. Arabidopsis profilins are functionally similar to yeast profilins: identification of a vascular bundle-specific profilin and a pollen-specific profilin.
    Plant J. 1996 Aug;10(2):269-79 PMID: 8771785
  36. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility.
    J Cell Biol. 1997 Mar 24;136(6):1307-22 PMID: 9087445
  37. The maize actin-depolymerizing factor, ZmADF3, redistributes to the growing tip of elongating root hairs and can be induced to translocate into the nucleus with actin.
    Plant J. 1997 Nov;12(5):1035-43 PMID: 9418045
  38. Control of actin dynamics.
    Curr Opin Cell Biol. 1998 Feb;10(1):45-51 PMID: 9484594
  39. How ADF/cofilin depolymerizes actin filaments.
    Curr Opin Cell Biol. 1998 Feb;10(1):140-4 PMID: 9484606
  40. Gelsolin is a downstream effector of rac for fibroblast motility.
    EMBO J. 1998 Mar 2;17(5):1362-70 PMID: 9482733
  41. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase.
    Nature. 1998 Jun 25;393(6687):805-9 PMID: 9655397
  42. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization.
    Nature. 1998 Jun 25;393(6687):809-12 PMID: 9655398
  43. 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
  44. The effect of two actin depolymerizing factors (ADF/cofilins) on actin filament turnover: pH sensitivity of F-actin binding by human ADF, but not of Acanthamoeba actophorin.
    Eur J Biochem. 1998 Sep 1;256(2):388-97 PMID: 9760179
  45. XAIP1: a Xenopus homologue of yeast actin interacting protein 1 (AIP1), which induces disassembly of actin filaments cooperatively with ADF/cofilin family proteins.
    J Cell Sci. 1999 May;112 ( Pt 10):1553-65 PMID: 10212149
  46. Cooperation of two actin-binding proteins, cofilin and Aip1, in Saccharomyces cerevisiae.
    Genes Cells. 1999 Jan;4(1):21-32 PMID: 10231390
  47. Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip.
    J Cell Biol. 1999 Feb 8;144(3):483-96 PMID: 9971743
  48. Aip1p interacts with cofilin to disassemble actin filaments.
    J Cell Biol. 1999 Jun 14;145(6):1251-64 PMID: 10366597
  49. Hyperosmotic stress-induced reorganization of actin bundles in Dictyostelium cells over-expressing cofilin.
    Genes Cells. 1999 Jun;4(6):311-24 PMID: 10421841
  50. Actin-organelle interaction: association with chloroplast in arabidopsis leaf mesophyll cells.
    Cell Motil Cytoskeleton. 1999 Oct;44(2):110-8 PMID: 10506746
  51. Proteins of the ADF/cofilin family: essential regulators of actin dynamics.
    Annu Rev Cell Dev Biol. 1999;15:185-230 PMID: 10611961
  52. Regulating actin-filament dynamics in vivo.
    Trends Biochem Sci. 2000 Jan;25(1):19-23 PMID: 10637608
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.005363
Published
2002-11-00
Pages
2915-27
Language
English
Region
England
NLM ID
9208688
PMCID
PMC152736
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/E/J/00000129 · United Kingdom
External Links
PubMed source DOI: 10.1105/tpc.005363 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2