Skip to main content
SpringerLink
Log in

The Rac1 inhibitor, NSC23766, depolarizes adhesive secretion, endomembrane cycling, and tip growth in the fucoid alga, Silvetia compressa

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Proper cell morphogenesis is dependent on the establishment and expression of cellular polarity. In the fucoid zygote, cell shape is critical for establishing the developmental pattern of the adult, and is achieved by guiding insertion of new membrane and wall to the rhizoid tip. Selection and growth of the appropriate tip site are accompanied by formation of dynamic actin arrays associated with the actin-nucleating Arp2/3 complex. In eukaryotes, a major pathway for activation of the Arp2/3 complex is via the Rho family GTPase, Rac1, which stimulates the Scar/WAVE complex. To determine whether Rac1 controls actin nucleation in Silvetia compressa (J. Agardh) E. Serrao, T. O. Cho, S. M. Boo et Brawley, we tested the effects of the Rac1-specific inhibitory compound, NSC23766, on actin dependent processes and on actin arrays. We found that NSC23766 disrupted polar secretion of adhesive, polarization of endomembranes, and tip-focused growth in the rhizoid. Similarly, NSC23766 altered actin and Arp2 localization in the growing rhizoid. In contrast, NSC23766 had no effect on selection of the growth site or on cytokinesis. These data suggest that Rac1 participates in nucleation of specific actin arrays in the developing zygote.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AF:

After fertilization

NSC:

NSC23766 (Rac1 inhibitor)

References

  • Alessa L, Kropf DL (1999) F-actin marks the rhizoid pole in living Pelvetia compressa zygotes. Development 126:201–209

    PubMed  CAS  Google Scholar 

  • Basu D, Le J, El-Din El-Assal S, Huang S, Zhang C, Mallery EL, Koliantz G, Staiger CJ, Szymanski DB (2005) DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17:502–524

    Article  PubMed  Google Scholar 

  • Bear J, Rawls J, Saxe C III (1998) SCAR, a WASP-related protein, isolated as a suppressor of receptor defects in late Dictyostelium development. J Cell Biol 142:1325–1335

    Article  PubMed  CAS  Google Scholar 

  • Bisgrove SR, Henderson DC, Kropf DL (2003) Asymmetric division in fucoid zygotes is positioned by telophase nuclei. Plant Cell 15:854–862

    Article  PubMed  CAS  Google Scholar 

  • Bisgrove SR, Kropf DL (2004) Cytokinesis in brown algae: studies of asymmetric division in fucoid zygotes. Protoplasma 223:163–173

    Article  PubMed  CAS  Google Scholar 

  • Bouget F-Y, Gerttula S, Shaw SL, Quatrano RS (1996) Localization of actin mRNA during the establishment of cell polarity and early cell divisions in Fucus embryos. Plant Cell 8:189–201

    Article  PubMed  CAS  Google Scholar 

  • Brembu T, Winge P, Bones A (2005) Catching the WAVEs of plant actin regulation. J Plant Growth Regul 24:55–66

    Article  CAS  Google Scholar 

  • Brembu T, Winge P, Bones A, Yang Z (2006) A RHOse by any other name: a comparitive analysis of animal and plant Rho GTPases. Cell Res 16:435–445

    Article  PubMed  CAS  Google Scholar 

  • Brembu T, Winge P, Seem M, Bones A (2004) NAPP and PIRP encode subunits of a putative wave regulatory protein complex involved in plant cell morphogenesis. Plant Cell 16:2335–2349

    Article  PubMed  CAS  Google Scholar 

  • Brownlee C, Bouget F-Y, Corellou F (2001) Choosing sides: establishment of polarity in zygotes of fucoid algae. Semin Cell Dev Biol 12:345–351

    Article  PubMed  CAS  Google Scholar 

  • Deeks M, Kaloriti D, Davies B, Malho R, Hussey P (2004) Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr Biol 14:1410–1414

    Article  PubMed  CAS  Google Scholar 

  • Eden S, Rohatgi R, Podtelejnikov A, Mann M, Kirschner M (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790–793

    Article  PubMed  CAS  Google Scholar 

  • El-Din El-Assal S, Le J, Basu D, Mallery E, Szymanski D (2004) Arabidopsis GNARLED encodes a NAP125 homolog that positively regulates Arp2/3. Curr Biol 14:1405–1409

    Article  Google Scholar 

  • Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629–635

    Article  PubMed  CAS  Google Scholar 

  • Fowler J, Vejlupkova Z, Goodner B, Lu G, Quatrano R (2004) Localization to the rhizoid tip implicates a Fucus distichus Rho family GTPase in a conserved cell polarity pathway. Planta 219:856–866

    Article  PubMed  CAS  Google Scholar 

  • Frank M, Egile C, Dyachok J, Djakovic S, Nolasco M, Li R, Smith L (2004) Activation of Arp2/3 complex-dependent actin polymerization by plant proteins distantly related to Scar/WAVE. Proc Natl Acad Sci USA 101:16379–16384

    Article  PubMed  CAS  Google Scholar 

  • Frank M, Smith L (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12:849–853

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 101:7618–7623

    Article  PubMed  CAS  Google Scholar 

  • Gautreau A, Ho HH, Li J, Steen H, Gygi S, Kirschner MW (2004) Purification and architecture of the ubiquitous wave complex. Proc Natl Acad Sci USA 101:4379–4383

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hable W, Kropf D (2005) The Arp2/3 complex nucleates actin arrays during zygote polarity establishment and growth. Cell Motil Cytoskeleton 61:9–20

    Article  PubMed  CAS  Google Scholar 

  • Hable WE, Kropf DL (1998) Roles of secretion and the cytoskeleton in cell adhesion and polarity establishment in Pelvetia compressa zygotes. Dev Biol 198:45–56

    PubMed  CAS  Google Scholar 

  • Hable WE, Kropf DL (2000) Sperm entry induces polarity in fucoid zygotes. Development 127:493–501

    PubMed  CAS  Google Scholar 

  • Hable WE, Miller NR, Kropf DL (2003) Polarity establishment requires dynamic actin in fucoid zygotes. Protoplasma 221:193–204

    PubMed  CAS  Google Scholar 

  • Hadley R, Hable W, Kropf D (2006) Polarization of the endomembrane system is an early event in fucoid zygote development. BMC Plant Biol 6:1–10

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Innocenti M, Zucconi A, Disanza A, Frittoli E, Areces L (2004) Abil is essential for the formation and activation of a WAVE2 signalling complex. Nat Cell Biol 6:319–327

    Article  PubMed  CAS  Google Scholar 

  • Jaffe LF (1958) Tropistic responses of zygotes of the Fucaceae to polarized light. Exp Cell Res 15:282–299

    Article  PubMed  CAS  Google Scholar 

  • Jaffe LF (1968) Localization in the developing Fucus egg and the general role of localizing currents. Adv Morphol 7:295–328

    CAS  Google Scholar 

  • Ketelaar T, de Ruijter NCA, Emons AMC (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285–292

    Article  PubMed  CAS  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 regulated polar pollen tube growth. J Cell Biol 145:317–330

    Article  PubMed  CAS  Google Scholar 

  • Kropf DL (1997) Induction of polarity in fucoid zygotes. Plant Cell 9:1011–1020

    Article  PubMed  CAS  Google Scholar 

  • Kropf DL, Bisgrove SR, Hable WE (1999) Establishing a growth axis in fucoid algae. Trend Plant Sci 4:490–494

    Article  Google Scholar 

  • Le J, El-Din El-Assal S, Basu D, Saad M, Szymanski D (2003) Requirements for Arabidposis ATARP2 and ATARP3 during epidermal development. Curr Biol 13:1341–1347

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132:2034–2044

    Article  PubMed  CAS  Google Scholar 

  • Mathur J, Mathur N, Kernebeck B, Hulskamp M (2003a) Mutations in Actin-Related Proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15:1632–1645

    Article  PubMed  CAS  Google Scholar 

  • Mathur J, Mathur N, Kirik V, Kemebeck B, Purushottam S, Hulskamp M (2003b) Arabidopsis CROOKED encodes for the smallest subunit of the Arp2/3 complex and controls cell shape by region specific fine F-actin formation. Development 130:3137–3146

    Article  PubMed  CAS  Google Scholar 

  • Nibau C, Wu H-m, Cheung A (2006) RAC/ROP GTPases: ‘hubs’ for signal integration and diversification in plants. Trend Plant Sci 11:309–315

    Article  CAS  Google Scholar 

  • Pollard TD, Borisy Gg (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465

    Article  PubMed  CAS  Google Scholar 

  • Pu R, Wozniak M, Robinson KR (2000) Cortical actin filaments form rapidly during photopolarization and are required for the development of calcium gradients in Pelvetia compressa zygotes. Dev Biol 222:440–449

    Article  PubMed  CAS  Google Scholar 

  • Quatrano RS (1973) Separation of processes associated with differentiation of two-celled Fucus embryos. Dev Biol 30:209–213

    Article  PubMed  CAS  Google Scholar 

  • Quatrano RS, Shaw SL (1997) Role of the cell wall in the determination of cell polarity and the plane of cell division in Fucus embryos. Trend Plant Sci 2:15–21

    Article  Google Scholar 

  • Ridley A (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trend Cell Biol 16:522–529

    Article  CAS  Google Scholar 

  • Serrao EA, Lawrence AA, Brawley SH (1999) Evolution of the Fucaceae (Phaeophyceae) in ferred from nrDNA-ITS. J Phycol 35:382–394

    Article  Google Scholar 

  • Smith L, Li R (2004) Actin polymerization: riding the wave. Curr Biol 14:109–111

    Article  Google Scholar 

  • Stradal T, Scita G (2006) Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol 18:4–10

    Article  PubMed  CAS  Google Scholar 

  • Szymanski D (2005) Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol 8:103–112

    Article  PubMed  CAS  Google Scholar 

  • Takenawa T, Miki H (2001) WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114:1801–1809

    PubMed  CAS  Google Scholar 

  • Vreeland V, Waite JH, Epstein L (1998) Polyphenols and oxidases in substratum adhesion by marine algae and mussels. J Phycol 34:1–8

    Article  CAS  Google Scholar 

  • Welch MD (2002) Cellular control of actin nucleation. Annu Rev Cell Dev Biol 18:247–288

    Article  PubMed  CAS  Google Scholar 

  • Yoon H, Hackett J, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Darryl Kropf and Nick Peters for many helpful discussions during a summer research visit by W. E. H. This research was supported by the University of Massachusetts Dartmouth and by a Research Opportunity Award from the National Science Foundation to W. E. H. and Darryl L. Kropf IBN 0414089.

Author information

Authors and Affiliations

  1. Department of Biology, University of Massachusetts Dartmouth, 285 Old Westport Road, North Dartmouth, MA, 02747-2300, USA

    Whitney E. Hable, Sriharshan Reddy & Lindsay Julien

Authors
  1. Whitney E. Hable
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sriharshan Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lindsay Julien
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Whitney E. Hable.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hable, W.E., Reddy, S. & Julien, L. The Rac1 inhibitor, NSC23766, depolarizes adhesive secretion, endomembrane cycling, and tip growth in the fucoid alga, Silvetia compressa . Planta 227, 991–1000 (2008). https://doi.org/10.1007/s00425-007-0673-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0673-1

Keywords

Search

Navigation