Skip to main content
SpringerLink
Log in

Actin organization and regulation during pollen tube growth

  • Review
  • Published:
Frontiers in Biology

Abstract

Pollen is the male gametophyte of seed plants and its tube growth is essential for successful fertilization. Mounting evidence has demonstrated that actin organization and regulation plays a central role in the process of its germination and polarized growth. The native structures and dynamics of actin are subtly modulated by many factors among which numerous actin binding proteins (ABPs) are the most direct and significant regulators. Upstream signals such as Ca2+, PIP2 (phosphatidylinositol-4,5-bis-phosphate) and GTPases can also indirectly act on actin organization through several ABPs. Under such elaborate regulation, actin structures show dynamically continuous modulation to adapt to the in vivo biologic functions to mediate secretory vesicle transportation and fusion, which lead to normal growth of the pollen tube. Many encouraging progress has been made in the connection between actin regulation and pollen tube growth in recent years. In this review, we summarize different factors that affect actin organization in pollen tube growth and highlight relative research progress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allwood E G, Anthony R G, Smertenko A P, Reichelt S, Drøbak B K, Doonan J H, Weeds A G, Hussey P J (2002). Regulation of the pollen-specific actin-depolymerizing factor LlADF1. Plant Cell, 14(11): 2915–2927

    CAS  PubMed  Google Scholar 

  • Anderson R A, Boronenkov I V, Doughman S D, Kunz J, Loijens J C (1999). Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J Biol Chem, 274(15): 9907–9910

    CAS  PubMed  Google Scholar 

  • Andrianantoandro E, Pollard T D (2006). Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell, 24(1): 13–23

    CAS  PubMed  Google Scholar 

  • Bamburg J R, Bernstein B W (2008). ADF/cofilin. Curr Biol, 18(7): R273–R275

    CAS  PubMed  Google Scholar 

  • Bar-Sagi D, Hall A (2000). Ras and Rho GTPases: a family reunion. Cell, 103(2): 227–238

    CAS  PubMed  Google Scholar 

  • Bedinger P (1992). The remarkable biology of pollen. Plant Cell, 4(8): 879–887

    CAS  PubMed  Google Scholar 

  • Blanchoin L, Pollard T D (1999). Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments. J Biol Chem, 274(22): 15538–15546

    CAS  PubMed  Google Scholar 

  • Blanchoin L, Staiger C J (2010). Plant formins: diverse isoforms and unique molecular mechanism. Biochim Biophys Acta, 1803(2): 201–206

    CAS  PubMed  Google Scholar 

  • Cai G, Cresti M (2008). Organelle motility in the pollen tube: a tale of 20 years. J Exp Bot, Page 1 of 15

  • Cárdenas L, Lovy-Wheeler A, Kunkel J G, Hepler P K (2008). Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol, 146(4): 1611–1621

    PubMed  Google Scholar 

  • Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia G X, Hong Y, Chua N H, Pantaloni D (1997). Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol, 136(6): 1307–1322

    CAS  PubMed  Google Scholar 

  • Chalkia D, Nikolaidis N, Makalowski W, Klein J, Nei M (2008). Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol Biol Evol, 25(12): 2717–2733

    CAS  PubMed  Google Scholar 

  • Chaudhry F, Guérin C, von Witsch M, Blanchoin L, Staiger C J (2007). Identification of Arabidopsis cyclase-associated protein 1 as the first nucleotide exchange factor for plant actin. Mol Biol Cell, 18(8): 3002–3014

    CAS  PubMed  Google Scholar 

  • Chen C Y, Cheung A Y, Wu H M (2003). Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell, 15(1): 237–249

    CAS  PubMed  Google Scholar 

  • Chen C Y, Wong E I, Vidali L, Estavillo A, Hepler P K, Wu H M, Cheung A Y (2002). The regulation of actin organization by actindepolymerizing factor in elongating pollen tubes. Plant Cell, 14(9): 2175–2190

    CAS  PubMed  Google Scholar 

  • Chen H, Bernstein B W, Sneider J M, Boyle J A, Minamide L S, Bamburg J R (2004). In vitro activity differences between proteins of the ADF/cofilin family define two distinct subgroups. Biochemistry, 43(22): 7127–7142

    CAS  PubMed  Google Scholar 

  • Chen T, Wu X, Chen Y, Li X, Huang M, Zheng M, Baluska F, Samaj J, Lin J (2009). Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth. Plant Physiol, 149(2): 1111–1126

    CAS  PubMed  Google Scholar 

  • Cheung A Y, Duan Q H, Costa S S, de Graaf B H, Di Stilio V S, Feijo J, Wu H M (2008). The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubule-binding reporter proteins. Mol Plant, 1(4): 686–702

    CAS  PubMed  Google Scholar 

  • Cheung A Y, Niroomand S, Zou Y J, Wu HM (2010). A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc Natl Acad Sci USA, 107(37): 16390–16395

    CAS  PubMed  Google Scholar 

  • Cheung A Y, Wu H M (2004). Overexpression of an Arabidopsis forming stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell, 16(1): 257–269

    CAS  PubMed  Google Scholar 

  • Cheung A Y, Wu H M (2007). Structural and functional compartmentalization in pollen tubes. J Exp Bot, 58(1): 75–82

    CAS  PubMed  Google Scholar 

  • Cheung A Y, Wu H M (2008). Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol, 59(1): 547–572

    CAS  PubMed  Google Scholar 

  • Cooper J A, Sept D (2008). New insights into mechanism and regulation of actin capping protein. Int Rev Cell Mol Biol, 267: 183–206

    CAS  PubMed  Google Scholar 

  • Cremona O, Di Paolo G, Wenk M R, Lüthi A, Kim W T, Takei K, Daniell L, Nemoto Y, Shears S B, Flavell R A, McCormick D A, De Camilli P (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell, 99(2): 179–188

    CAS  PubMed  Google Scholar 

  • Cvrcková F, Rivero F, Bavlnka B (2004). Evolutionarily conserved modules in actin nucleation: lessons from Dictyostelium discoideum and plants. Review article. Protoplasma, 224(1–2): 15–31

    Google Scholar 

  • Dawson A P (1997). Calcium signalling: how do IP3 receptors work? Curr Biol, 7(9): R544–R547

    CAS  PubMed  Google Scholar 

  • de Graaf B H J, Cheung A Y, Andreyeva T, Levasseur K, Kieliszewski M, Wu H M (2005). Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell, 17(9): 2564–2579

    PubMed  Google Scholar 

  • Deeks MJ, Cvrcková F, Machesky LM, Mikitová V, Ketelaar T, Zársky V, Davies B, Hussey P J (2005). Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actinbinding proteins and cause defects in cell expansion upon aberrant expression. New Phytol, 168(3): 529–540

    CAS  PubMed  Google Scholar 

  • Deeks M J, Rodrigues C, Dimmock S, Ketelaar T, Maciver S K, Malhó R, Hussey P J (2007). Arabidopsis CAP1 — a key regulator of actin organisation and development. J Cell Sci, 120(Pt 15): 2609–2618

    CAS  PubMed  Google Scholar 

  • Derksen J, Rutten T, Van Amstel T, de Win A, Doris F, Steer M (1995). Regulation of pollen tube growth. Acta Bot. Neerl., 44: 93–119

    Google Scholar 

  • Dhonukshe P, Laxalt AM, Goedhart J, Gadella TWJ, Munnik T (2003). Phospholipase d activation correlates with microtubule reorganization in living plant cells. Plant Cell, 15(11): 2666–2679

    CAS  PubMed  Google Scholar 

  • Dowd P E, Coursol S, Skirpan A L, Kao T H, Gilroy S (2006). Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell, 18(6): 1438–1453

    CAS  PubMed  Google Scholar 

  • Drøbak B K, Watkins P A C, Valenta R, Dove S K, Lloyd CW, Staiger C J (1994). Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein, profilin. Plant J, 6(3): 389–400

    Google Scholar 

  • Faix J, Grosse R (2006). Staying in shape with formins. Dev Cell, 10(6): 693–706

    CAS  PubMed  Google Scholar 

  • Fan X, Hou J, Chen X, Chaudhry F, Staiger C J, Ren H Y (2004). Identification and characterization of a Ca2+-dependent actin filament-severing protein from lily pollen. Plant Physiol, 136(4): 3979–3989

    CAS  PubMed  Google Scholar 

  • Franklin-Tong V E (1999). Signaling and the modulation of pollen tube growth. Plant Cell, 11(4): 727–738

    CAS  PubMed  Google Scholar 

  • Franklin-Tong V E, Drøbak B K, Allan A C, Watkins P A C, Trewavas A J (1996). Growth of pollen tubes of Papaver rhoeas is regulated by a slow moving calcium wave propagated by inositol triphosphate. Plant Cell, 8(8): 1305–1321

    CAS  PubMed  Google Scholar 

  • Fu Y, Li H, Yang Z (2002). The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell, 14(4): 777–794

    CAS  PubMed  Google Scholar 

  • Fu Y, Wu G, Yang Z (2001). Rop GTPase-dependent dynamics of tiplocalized F-actin controls tip growth in pollen tubes. J Cell Biol, 152(5): 1019–1032

    CAS  PubMed  Google Scholar 

  • Geitmann A, Snowman B N, Emons A M C, Franklin-Tong V E (2000). Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. Plant Cell, 12(7): 1239–1251

    CAS  PubMed  Google Scholar 

  • Gibbon B C, Kovar D R, Staiger C J (1999). Latrunculin B has different effects on pollen germination and tube growth. Plant Cell, 11(12): 2349–2363

    CAS  PubMed  Google Scholar 

  • Gibbon B C, Zonia L E, Kovar D R, Hussey P J, Staiger C J (1998). Pollen profilin function depends on interaction with proline-rich motifs. Plant Cell, 10(6): 981–993

    CAS  PubMed  Google Scholar 

  • Goldschmidt-Clermont P J, Machesky L M, Baldassare J J, Pollard T D (1990). The actin-binding protein profilin binds to PIP2 and inhibits its hydrolysis by phospholipase C. Science, 247(4950): 1575–1578

    CAS  PubMed  Google Scholar 

  • Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z B (2005). A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol, 169(1): 127–138

    CAS  PubMed  Google Scholar 

  • Gu Y, Vernoud V, Fu Y, Yang Z (2003). ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot, 54(380): 93–101

    CAS  PubMed  Google Scholar 

  • Gu Y, Wang Z, Yang Z (2004). ROP/RAC GTPase: an old new master regulator for plant signaling. Curr Opin Plant Biol, 7(5): 527–536

    CAS  PubMed  Google Scholar 

  • Gungabissoon R A, Jiang C J, Drøbak B K, Maciver S K, Hussey P J (1998). Interaction of maize actin-depolymerising factor with actin and phosphoinositides and its inhibition of plant phospholipase C. Plant J, 16(6): 689–696

    CAS  Google Scholar 

  • Gungabissoon R A, Khan S, Hussey P J, Maciver S K (2001). Interaction of elongation factor 1alpha from Zea mays (ZmEF-1alpha) with Factin and interplay with the maize actin severing protein, ZmADF3. Cell Motil Cytoskeleton, 49(2): 104–111

    CAS  PubMed  Google Scholar 

  • Guo C Q, Ren H Y (2006). Formins: bringing new insights to the organization of actin cytoskeleton. Chin Sci Bull, 51(24): 2937–2943

    CAS  Google Scholar 

  • Harris E S, Higgs H N (2004). Actin cytoskeleton: formins lead the way. Curr Biol, 14(13): R520–R522

    CAS  PubMed  Google Scholar 

  • Harris E S, Rouiller I, Hanein D, Higgs H N (2006). Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J Biol Chem, 281(20): 14383–14392

    CAS  PubMed  Google Scholar 

  • Helling D, Possart A, Cottier S, Klahre U, Kost B (2006). Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell, 18(12): 3519–3534

    CAS  PubMed  Google Scholar 

  • Hepler P K, Vidali L, Cheung A Y (2001). Polarized cell growth in higher plants. Annu Rev Cell Dev Biol, 17(1): 159–187

    CAS  PubMed  Google Scholar 

  • Higashida C, Miyoshi T, Fujita A, Oceguera-Yanez F, Monypenny J, Andou Y, Narumiya S, Watanabe N (2004). Actin polymerizationdriven molecular movement of mDia1 in living cells. Science, 303(5666): 2007–2010

    CAS  PubMed  Google Scholar 

  • Holdaway-Clarke T L, Feijo J A, Hackett G R, Kunkel J G, Hepler P K (1997). Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell, 9(11): 1999–2010

    CAS  PubMed  Google Scholar 

  • Hong Z, Staiculescu M, Sun M, Levitan I, Forgacs G (2009). How phosphatidylinositol 4,5-bisphosphate regulates membrane-cytoskeleton interaction in endothelial cells? Biophysical Journal, 96: 395a

    Google Scholar 

  • Hormanseder K, Obermeyer G, Foissner I (2005). Disturbance of endomembrane trafficking by brefeldin A and calyculin A reorganizes the actin cytoskeleton of Lilium longiflorum pollen tubes. Protoplasma, 227: 25–36

    CAS  PubMed  Google Scholar 

  • Huang S, Blanchoin L, Chaudhry F, Franklin-Tong V E, Staiger C J (2004). A gelsolin-like protein from Papaver rhoeas pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. J Biol Chem, 279(22): 23364–23375

    CAS  PubMed  Google Scholar 

  • Huang S, Blanchoin L, Kovar D R, Staiger C J (2003). Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J Biol Chem, 278(45): 44832–44842

    CAS  PubMed  Google Scholar 

  • Huang S, Gao L, Blanchoin L, Staiger C J (2006). Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Mol Biol Cell, 17(4): 1946–1958

    CAS  PubMed  Google Scholar 

  • Huang S, Robinson R C, Gao L Y, Matsumoto T, Brunet A, Blanchoin L, Staiger C J (2005). Arabidopsis VILLIN1 generates actin filament cables that are resistant to depolymerization. Plant Cell, 17(2): 486–501

    CAS  PubMed  Google Scholar 

  • Hussey P J, Ketelaar T, Deeks M J (2006). Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol, 57(1): 109–125

    CAS  PubMed  Google Scholar 

  • Hwang J U, Vernoud V, Szumlanski A, Nielsen E, Yang Z (2008). A tiplocalized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr Biol, 18(24): 1907–1916

    CAS  PubMed  Google Scholar 

  • Ingouff M, Fitz Gerald J N, Guérin C, Robert H, Sørensen M B, Van Damme D, Geelen D, Blanchoin L, Berger F (2005). Plant forming AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat Cell Biol, 7(4): 374–380

    CAS  PubMed  Google Scholar 

  • Khurana P, Henty J L, Huang S J, Staiger A M, Blanchoin L, Staiger C J (2010). Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell, 22(8): 2727–2748

    CAS  PubMed  Google Scholar 

  • Kim S R, Kim Y W, An G (1993). Molecular cloning and characterization of anther-preferential cDNA encoding a putative actin-depolymerizing factor. Plant Mol Biol, 21(1): 39–45

    CAS  PubMed  Google Scholar 

  • Klahre U, Friederich E, Kost B, Louvard D, Chua N H (2000). Villin-like actin-binding proteins are expressed ubiquitously in Arabidopsis. Plant Physiol, 122(1): 35–48

    CAS  PubMed  Google Scholar 

  • Kost B (2008). Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol, 18(3): 119–127

    CAS  PubMed  Google Scholar 

  • Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N H (1999). Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol, 145(2): 317–330

    CAS  PubMed  Google Scholar 

  • Kost B, Spielhofer P, Chua N H (1998). A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J, 16(3): 393–401

    CAS  PubMed  Google Scholar 

  • Kovar D R (2006). Molecular details of formin-mediated actin assembly. Curr Opin Cell Biol, 18(1): 11–17

    CAS  PubMed  Google Scholar 

  • Kovar D R, Yang P, Sale W S, Drøbak B K, Staiger C J (2001). Chlamydomonas reinhardtii produces a profilin with unusual biochemical properties. J Cell Sci, 114(Pt 23): 4293–4305

    CAS  PubMed  Google Scholar 

  • Kreis T, Vale R (1999). Guidebook to the cytoskeletal and motor proteins. New York: Oxford University Press

    Google Scholar 

  • Kühtreiber W M, Jaffe L F (1990). Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol, 110(5): 1565–1573

    PubMed  Google Scholar 

  • Lee Y J, Szumlanski A, Nielsen E, Yang Z B (2008). Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J Cell Biol, 181(7): 1155–1168

    CAS  PubMed  Google Scholar 

  • Li H, Lin Y, Heath R M, Zhu M X, Yang Z (1999). Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell, 11(9): 1731–1742

    CAS  PubMed  Google Scholar 

  • Li H, Wu G, Ware D, Davis K R, Yang Z (1998). Arabidopsis Rhorelated GTPases: differential gene expression in pollen and polar localization in fission yeast. Plant Physiol, 118(2): 407–417

    CAS  PubMed  Google Scholar 

  • Li Y H, Shen Y, Cai C, Zhong C C, Zhu L, Yuan M, Ren H Y (2010). The type II Arabidopsis formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell, 22(8): 2710–2726

    CAS  PubMed  Google Scholar 

  • Lord E M, Russell S D (2002). The mechanisms of pollination and fertilization in plants. Annu Rev Cell Dev Biol, 18(1): 81–105

    CAS  PubMed  Google Scholar 

  • Lord E M, Walling L L, Jauh G Y (1996). Cell adhesion in plants and its role in pollination. In: Smallwood M, Knox J P, Bowles D J, eds. Membranes: specialized functions in plants. Oxford, UK: BIOS Scientific Publishers, 21–38

    Google Scholar 

  • Lovy-Wheeler A, Cárdenas L, Kunkel J G, Hepler P K (2007). Differential organelle movement on the actin cytoskeleton in lily pollen tubes. Cell Motil Cytoskeleton, 64(3): 217–232

    PubMed  Google Scholar 

  • Lovy-Wheeler A, Kunkel J G, Allwood E G, Hussey P J, Hepler P K (2006). Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell, 18(9): 2182–2193

    CAS  PubMed  Google Scholar 

  • Lovy-Wheeler A, Wilsen K L, Baskin T I, Hepler P K (2005). Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta, 221(1): 95–104

    CAS  PubMed  Google Scholar 

  • Maciver S K, Hussey P J (2002). The ADF/cofilin family: actinremodeling proteins. Genome Biol, 3(5): 3007.1–3007.12

    Google Scholar 

  • Malhó R (1998). The role of inositol(1,4,5)triphosphate in pollen tube growth and orientation. Sex Plant Reprod, 11: 231–235

    Google Scholar 

  • Malhó R, Liu Q, Monteiro D, Rato C, Camacho L, Dinis A (2006). Signalling pathways in pollen germination and tube growth. Protoplasma, 228(1–3): 21–30

    PubMed  Google Scholar 

  • Malhó R, Read N D, Pais M, Trewavas A J (1994). Role of cytosolic calcium in the reorientation of pollen tube growth. Plant J, 5(3): 331–341

    Google Scholar 

  • Malhó R, Read N D, Trewavas A J, Pais M S (1995). Calcium channel activity during pollen tube growth and reorientation. Plant Cell, 7(8): 1173–1184

    PubMed  Google Scholar 

  • Malhó R, Trewavas A J (1996). Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell, 8(11): 1935–1949

    PubMed  Google Scholar 

  • Martin T F J (1998). Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol, 14(1): 231–264

    CAS  PubMed  Google Scholar 

  • Mascarenhas J P (1993). Molecular mechanisms of pollen tube growth and differentiation. Plant Cell, 5(10): 1303–1314

    CAS  PubMed  Google Scholar 

  • Mathur J (2005). Conservation of boundary extension mechanisms between plants and animals. J Cell Biol, 168(5): 679–682

    CAS  PubMed  Google Scholar 

  • Messerli M, Robinson K R (1997). Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J Cell Sci, 110(Pt 11): 1269–1278

    CAS  PubMed  Google Scholar 

  • Michelot A, Guérin C, Huang S J, Ingouff M, Richard S, Rodiuc N, Staiger C J, Blanchoin L (2005). The formin homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis FORMIN1. Plant Cell, 17(8): 2296–2313

    CAS  PubMed  Google Scholar 

  • Molendijk A J, Bischoff F, Rajendrakumar C S V, Friml J, Braun M, Gilroy S, Palme K (2001). Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J, 20(11): 2779–2788

    CAS  PubMed  Google Scholar 

  • Monteiro D, Castanho Coelho P, Rodrigues C, Camacho L, Quader H, Malhó R (2005a). Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids. Protoplasma, 226(1–2): 31–38

    CAS  PubMed  Google Scholar 

  • Monteiro D, Liu Q, Lisboa S, Scherer G E F, Quader H, Malhó R (2005b). Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. J Exp Bot, 56(416): 1665–1674

    CAS  PubMed  Google Scholar 

  • Moseley J B, Goode B L (2005). Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J Biol Chem, 280(30): 28023–28033

    CAS  PubMed  Google Scholar 

  • Munnik T (2001). Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci, 6(5): 227–233

    CAS  PubMed  Google Scholar 

  • Nakayasu T, Yokota E, Shimmen T (1998). Purification of an actinbinding protein composed of 115-kDa polypeptide from pollen tubes of lily. Biochem Biophys Res Commun, 249(1): 61–65

    CAS  PubMed  Google Scholar 

  • O’Luanaigh N, Pardo R, Fensome A, Allen-Baume V, Jones D, Holt M R, Cockcroft S (2002). Continual production of phosphatidic acid by phospholipase D is essential for antigen-stimulated membrane ruffling in cultured mast cells. Mol Biol Cell, 13(10): 3730–3746

    PubMed  Google Scholar 

  • Okreglak V, Drubin D G (2010). Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway. J Cell Biol, 188(6): 769–777

    CAS  PubMed  Google Scholar 

  • Perelroizen I, Didry D, Christensen H, Chua N H, Carlier M F (1996). Role of nucleotide exchange and hydrolysis in the function of profiling in action assembly. J Biol Chem, 271(21): 12302–12309

    CAS  PubMed  Google Scholar 

  • Pierson E S, Miller D D, Callaham D A, Shipley AM, Rivers B A, Cresti M, Hepler P K (1994). 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, 6(12): 1815–1828

    CAS  PubMed  Google Scholar 

  • Pina C, Pinto F, Feijó J A, Becker J D (2005). Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol, 138(2): 744–756

    CAS  PubMed  Google Scholar 

  • Pollard T D, Blanchoin L, Mullins R D (2000). Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct, 29(1): 545–576

    CAS  PubMed  Google Scholar 

  • Powner D J, Wakelam M J O (2002). The regulation of phospholipase D by inositol phospholipids and small GTPases. FEBS Lett, 531(1): 62–64

    CAS  PubMed  Google Scholar 

  • Rathore K S, Cork R J, Robinson K R (1991). A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Dev Biol, 148(2): 612–619

    CAS  PubMed  Google Scholar 

  • Rato C, Monteiro D, Hepler P K, Malhó R (2004). Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. Plant J, 38(6): 887–897

    CAS  PubMed  Google Scholar 

  • Raucher D, Stauffer T, Chen W, Shen K, Guo S, York J D, Sheetz M P, Meyer T (2000). Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell, 100(2): 221–228

    CAS  PubMed  Google Scholar 

  • Ren H Y, Xiang Y (2007). The function of actin-binding proteins in pollen tube growth. Protoplasma, 230(3–4): 171–182

    CAS  PubMed  Google Scholar 

  • Ruzicka D R, Kandasamy M K, McKinney E C, Burgos-Rivera B, Meagher R B (2007). The ancient subclasses of Arabidopsis actin depolymerizing factor genes exhibit novel and differential expression. Plant J, 52(3): 460–472

    CAS  PubMed  Google Scholar 

  • Sagot I, Klee S K, Pellman D (2002). Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat Cell Biol, 4(1): 42–50

    CAS  PubMed  Google Scholar 

  • Snowman B N, Kovar D R, Shevchenko G, Franklin-Tong V E, Staiger C J (2002). Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell, 14(10): 2613–2626

    CAS  PubMed  Google Scholar 

  • Staiger C J, Blanchoin L (2006). Actin dynamics: old friends with new stories. Curr Opin Plant Biol, 9(6): 554–562

    CAS  PubMed  Google Scholar 

  • Staiger C J, Hussey P J (2004). Actin and actin-modulating proteins. In Hussey P J, ed. The Plant Cytoskeleton in Cell Differentiation and Development. Oxford: Blackwell Publishers, pp. 32–80

    Google Scholar 

  • Staiger C J, Poulter N S, Henty J L, Franklin-Tong V E, Blanchoin L (2010). Regulation of actin dynamics by actin-binding proteins in pollen. J Exp Bot, 61(7): 1969–1986

    CAS  PubMed  Google Scholar 

  • Staiger C J, Sheahan M B, Khurana P, Wang X, McCurdy D W, Blanchoin L (2009). Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol, 184(2): 269–280

    CAS  PubMed  Google Scholar 

  • Steer M W, Steer J M (1989). Pollen tube tip growth. New Phytol, 111(3): 323–358

    Google Scholar 

  • Stevenson J M, Perera I Y, Heilmann I, Persson S, Boss W F (2000). Inositol signaling and plant growth. Trends Plant Sci, 5(6): 252–258

    CAS  PubMed  Google Scholar 

  • Sweeney D A, Siddhanta A, Shields D (2002). Fragmentation and reassembly of the Golgi apparatus in vitro. A requirement for phosphatidic acid and phosphatidylinositol 4,5-bisphosphate synthesis. J Biol Chem, 277(4): 3030–3039

    CAS  PubMed  Google Scholar 

  • Sze H, Li X, Palmgren M G (1999). Energization of plant cell membranes by H+-pumping ATPases. Regulation and biosynthesis. Plant Cell, 11(4): 677–690

    CAS  PubMed  Google Scholar 

  • Szymanski D B, Cosgrove D J (2009). Dynamic co-ordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol, 19(17): 800–811

    Google Scholar 

  • Tao Z H, Ren H Y (2003) Regulation of gelsolin to plant actin filaments and its distribution in pollen. Science in China, 46(4): 379–388

    CAS  PubMed  Google Scholar 

  • Thomas C, Tholl S, Moes D, Dieterle M, Papuga J, Moreau F, Steinmetz A (2009). Actin bundling in plants. Cell Motil Cytoskeleton, 66(11): 940–957

    CAS  PubMed  Google Scholar 

  • Thomas S G, Huang S, Li S, Staiger C J, Franklin-Tong V E (2006). Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol, 174(2): 221–229

    CAS  PubMed  Google Scholar 

  • Valenta R, Duchêne M, Pettenburger K, Sillaber C, Valent P, Bettelheim P, Breitenbach M, Rumpold H, Kraft D, Scheiner O (1991). Identification of profilin as a novel pollen allergen; IgE autoreactivity in sensitized individuals. Science, 253(5019): 557–560

    CAS  PubMed  Google Scholar 

  • Valenta R, Ferreira F, Grote M, Swoboda I, Vrtala S, Duchêne M, Deviller P, Meagher R B, McKinney E, Heberle-Bors E (1993). Identification of profilin as an actin-binding protein in higher plants. J Biol Chem, 268(30): 22777–22781

    CAS  PubMed  Google Scholar 

  • Vavylonis D, Wu J Q, Hao S, O’Shaughnessy B, Pollard T D (2008). Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science, 319(5859): 97–100

    CAS  PubMed  Google Scholar 

  • Vernoud V, Horton A C, Yang Z, Nielsen E (2003). Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol, 131(3): 1191–1208

    CAS  PubMed  Google Scholar 

  • Vidali L, Hepler P K (1997). Characterization and localization of profiling in pollen grains and tubes of Lilium longiflorum. Cell Motil Cytoskeleton, 36(4): 323–338

    CAS  PubMed  Google Scholar 

  • Vidali L, McKenna S T, Hepler P K (2001). Actin polymerization is essential for pollen tube growth. Mol Biol Cell, 12(8): 2534–2545

    CAS  PubMed  Google Scholar 

  • Vidali L, Rounds C M, Hepler P K, Bezanilla M, Baxter I (2009). Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS ONE, 4(5): e5744

    PubMed  Google Scholar 

  • Wang T, Xiang Y, Hou J, Ren H Y (2008). ABP41 is involved in the pollen tube development via fragmenting actin filaments. Mol Plant, 1(6): 1048–1055

    CAS  PubMed  Google Scholar 

  • Way M, Weeds A (1988). Nucleotide sequence of pig plasma gelsolin. Comparison of protein sequence with human gelsolin and other actin-severing proteins shows strong homologies and evidence for large internal repeats. J Mol Biol, 203(4): 1127–1133

    CAS  Google Scholar 

  • Wilsen K L, Lovy-Wheeler A, Voigt B, Menzel D, Kunkel J G, Hepler P K (2006). Imaging the actin cytoskeleton in growing pollen tubes. Sex Plant Reprod, 19(2): 51–62

    Google Scholar 

  • Wu G, Gu Y, Li S, Yang Z (2001). A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell, 13(12): 2841–2856

    CAS  PubMed  Google Scholar 

  • Wu W, Yan L F (1997). Identification of gelsolin by western blotting in maize pollen. Chin Sci Bull, 42: 1784–1786

    Google Scholar 

  • Xiang Y, Huang X, Wang T, Zhang Y, Liu Q, Hussey P J, Ren H (2007). ACTIN BINDING PROTEIN 29 from Lilium pollen plays an important role in dynamic actin remodeling. Plant Cell, 19(6): 1930–1946

    CAS  PubMed  Google Scholar 

  • Yang Z (2002). Small GTPases: versatile signaling switches in plants. Plant Cell, 14(Suppl): S375–S388

    CAS  PubMed  Google Scholar 

  • Ye J, Zheng Y, Yan A, Chen N, Wang Z, Huang S, Yang Z (2009). Arabidopsis Formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell, 21:3868–3884

    CAS  PubMed  Google Scholar 

  • Yi K X, Guo C Q, Chen D, Zhao B, Yang B, Ren H (2005). Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis. Plant Physiol, 138(2): 1071–1082

    CAS  PubMed  Google Scholar 

  • Yokota E, Muto S, Shimmen T (2000). Calcium-calmodulin suppresses the filamentous actin-binding activity of a 135-kilodalton actinbundling protein isolated from lily pollen tubes. Plant Physiol, 123(2): 645–654

    CAS  PubMed  Google Scholar 

  • Yokota E, Shimmen K T T, Shimmen T (1998). Actin-bundling protein isolated from pollen tubes of lily. Biochemical and immunocytochemical characterization. Plant Physiol, 116(4): 1421–1429

    CAS  PubMed  Google Scholar 

  • Yokota E, Shimmen T (1999). The 135-kDa actin-bundling protein from lily pollen tubes arranges F-actin into bundles with uniform polarity. Planta, 209(2): 264–266

    CAS  PubMed  Google Scholar 

  • Yokota E, Vidali L, Tominaga M, Tahara H, Orii H, Morizane Y, Hepler P K, Shimmen T (2003). Plant 115-kDa actin-filament bundling protein, P-115-ABP, is a homologue of plant villin and is widely distributed in cells. Plant Cell Physiol, 44(10): 1088–1099

    CAS  PubMed  Google Scholar 

  • Zhang H, Qu X L, Bao C C, Khurana P, Wang Q N, Xie Y R, Zheng Y Y, Chen N Z, Blanchoin L, Staiger C J, Huang S J (2010). Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell, 22(8): 2749–2767

    CAS  PubMed  Google Scholar 

  • Zheng Z L, Yang Z (2000). The Rrop GTPase switch turns on polar growth in pollen. Trends Plant Sci, 5(7): 298–303

    CAS  PubMed  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol, 136(1): 2621–2632

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Sciences, Beijing Normal University, Beijing, 100875, China

    Xiuhua Xue, Fei Du, Jinsheng Zhu & Haiyun Ren

Authors
  1. Xiuhua Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinsheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haiyun Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haiyun Ren.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xue, X., Du, F., Zhu, J. et al. Actin organization and regulation during pollen tube growth. Front. Biol. 6, 40–51 (2011). https://doi.org/10.1007/s11515-011-1110-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11515-011-1110-1

Keywords

Search

Navigation