Polarized growth: maintaining focus on the tip

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Tip growth, a spatially focused cell expansion, has been best characterized in two plant cell types: pollen tubes and root hairs. It has long been established that both cell types require three intracellular components for this process: a tip-high calcium gradient, a polarized actin cytoskeleton, and tip-directed vesicle trafficking. More recently, additional mechanistic parallels have been observed between the two cell types, including roles for ROP and Rab GTPase signaling, phosphoinositides, calcium-dependent protein kinases, and the exocyst. Uncovering pathways that control the three components is beginning to reveal a highly interconnected network, which we call the tip growth LENS (for localization enhancing network, self-sustaining), that coordinates the required cellular activities to allow regulated tip growth, and to maintain itself as the tip advances.

Introduction

Pollen tubes and root hairs, although differing in origin, function, wall composition, rate of growth, and ultimate fate, share a common morphological form. Developmentally that form arises from tip growth, in which all growth is focused on a single specialized region, the apex of the tip-growing cell. The process of tip growth appears deceptively simple: the components needed to add new plasma membrane and cell wall are delivered to the apex and added to the tip by secretory vesicles and the process of exocytosis. Underlying this basic process, however, is a complex, dynamic system that involves membrane cycling, polarized actin organization, and a tip-focused gradient of cytosolic Ca2+ (reviewed in [1, 2, 3, 4, 5, 6]). These essential components appear to be interconnected, coordinated, and regulated by an extensive network of signaling pathways involving calcium, phospholipids, small GTPases, reactive oxygen species (ROS), and protein kinases. The complexity of the system reflects the nature of its function, for the system must provide a mechanism for localizing secretion to the tip while also assuring that the mechanism itself is perpetuated, continuously re-localized forward to the advancing tip, and responsive to directional signals. The purpose of this review is to examine recent research on this tip-focusing molecular machine, which, for the sake of brevity, we are calling the tip growth LENS (for localization enhancing network, self-sustaining). The advances of the past few years allow us to paint an outline, in broad strokes, of how the LENS works to maintain the focus of growth at the apex.

The basic components of the tip growth LENS (i.e. membrane cycling, the gradient in actin dynamics, and the Ca2+ gradient), although not identical, appear remarkably similar in root hairs and pollen tubes (Figure 1). At the molecular level, the limited data available suggest that there are many parallels between the LENS of pollen tubes and that of root hairs, but there are also likely to be differences (Table 1). Given our incomplete understanding of each cell type, we find it advantageous to consider the two cell types together. Despite probable differences in molecular detail, what we learn about the LENS in one cell type should inform our questions about the LENS in the other.

Several topics that are relevant to an overall understanding of tip growth are beyond the scope of this review, but have recently been reviewed elsewhere. These include the guidance of tip growth by external cues [7, 8], the potential role of microtubules [9], the participation of non-calcium ion gradients and fluxes [10], pectin methylesterase in the pollen tube cell wall [11], and the regulation of actin dynamics by specific actin-binding proteins (ABPs) [12, 13]. Also not covered are mechanisms that act early in the secretory pathway [14], which appear to have a more indirect effect on the LENS.

Section snippets

Apical membrane trafficking: Rabs nab a role

The localization of cell expansion to a single region fundamentally depends upon a focused secretory pathway. Exocytosis is required near the expansion site to provide materials for the expansion of the plasma membrane and the assembly of new cell wall. However, because exocytosis adds plasma membrane in excess of that required for growth, it is inextricably intertwined with compensatory endocytosis and membrane cycling [2, 15]. The membrane-staining dyes FM4-64 and FM1-43 are rapidly

Phosphoinositides: the message in the membrane

Over and above the possible connection between Rab GTPases and PI-4K activity, other components of the tip LENS are being linked to phosphoinositide signaling, highlighting its importance in maintaining focused growth. PtdIns(4,5)P2 accumulates in the apical plasma membrane of growing pollen tubes and root hairs [5, 28], and its localized release (by photoactivation of a caged probe) can redirect pollen tube growth [29]. Certain PtdIns(4,5)P2 derivatives (e.g. phosphatidic acid [PA] and

Calcium: going with the flux

The tip-high Ca2+ gradient is coupled to an extracellular influx of Ca2+ that occurs predominantly in the apex [2, 10]. This influx oscillates, lagging behind the periodic rapid growth pulses of lily pollen tubes, which exhibit regular oscillations of rapid and slow growth. This behavior is consistent with the hypothesis that Ca2+ influx is tip-localized, in part because expansion at the tip during growth opens stretch-activated Ca2+ channels. Indeed, stretch-activated Ca2+ channels were

ROP GTPases: who regulates the regulator?

Members of the ROP/RAC family of small GTPases (a subset of the eukaryotic Rho class) occupy an important position in the tip growth LENS in both pollen tubes and root hairs [42]. Class-I ROP/RACs, which are prenylated for membrane association, localize to the plasma membrane at the apex of pollen tubes and root hairs, and to the tip cytoplasm. The mechanism that maintains this polarization has been unclear, although some data indicate that ROP activity promotes its own apical localization [43

Oscillating outcomes and the exocyst

ROP/RAC activity in the pollen tube promotes both tip-localized F-actin assembly (through the Rop-interactive CRIB-motif containing protein4 [RIC4]) and accumulation of tip-localized cytosolic Ca2+ (through another interactor, RIC3) [50]. Intriguingly, these two pathways counteract each other: RIC3-induced elevation of Ca2+ leads to disassembly of RIC4-induced F-actin and vice versa. Hwang et al. [51] addressed how ROP1 coordinates the pathways to promote the growth of a pollen tube tip that

Conclusions

Synthesizing recent work with earlier discoveries allows us to generate a model for the tip LENS (Figure 2). This model is an overview, lacking many details, but illustrating known and hypothesized connections between important LENS components. We believe that two general points can be drawn from this model. First, although obvious holes remain in testing for similarities between tip growth in pollen tubes and root hairs, the overall outline of the model supports the idea of parallel mechanisms

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank M Foss, M Ivanchenko, and Z Vejlupkova for comments on the manuscript, and the laboratory of V Zarsky for sharing unpublished data. Research in the JEF's laboratory is supported by the US National Science Foundation (NSF; grant #IBN–0420226). During the writing of this manuscript, JEF was supported at the US Environmental Protection Agency by a Senior Research Associateship from the National Research Council.

References (69)

  • R.J. Carol et al.

    Building a hair: tip growth in Arabidopsis thaliana root hairs

    Philos Trans R Soc Lond B Biol Sci

    (2002)
  • D. Monteiro et al.

    Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids

    Protoplasma

    (2005)
  • L.G. Smith et al.

    Spatial control of cell expansion by the plant cytoskeleton

    Annu Rev Cell Dev Biol

    (2005)
  • E.M. Lord

    Adhesion and guidance in compatible pollination

    J Exp Bot

    (2003)
  • B.J. Sieberer et al.

    Microtubules guide root hair tip growth

    New Phytol

    (2005)
  • T.L. Holdaway-Clarke et al.

    Control of pollen tube growth: role of ion gradients and fluxes

    New Phytol

    (2003)
  • M. Bosch et al.

    Pectin methylesterases and pectin dynamics in pollen tubes

    Plant Cell

    (2005)
  • P.J. Hussey et al.

    Control of the actin cytoskeleton in plant cell growth

    Annu Rev Plant Biol

    (2006)
  • Staiger CJ, Blanchoin L: Actin dynamics: old friends with new stories. Curr Opin Plant Biol 2006, 9:in...
  • U. Neumann et al.

    Protein transport in plant cells: in and out of the Golgi

    Ann Bot

    (2003)
  • R.M. Parton et al.

    Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes

    J Cell Sci

    (2001)
  • M. Ovecka et al.

    Endocytosis and vesicle trafficking during tip growth of root hairs

    Protoplasma

    (2005)
  • M.A. Jones et al.

    Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis

    Plant J

    (2006)
  • P.A. Hemsley et al.

    The TIP GROWTH DEFECTIVE1 S-acyl transferase regulates plant cell growth in Arabidopsis

    Plant Cell

    (2005)
  • E. Lalanne et al.

    SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis

    Plant Cell

    (2004)
  • A.J. Molendijk et al.

    Small GTPases in vesicle trafficking

    Curr Opin Plant Biol

    (2004)
  • V. Vernoud et al.

    Analysis of the small GTPase gene superfamily of Arabidopsis

    Plant Physiol

    (2003)
  • B.H. de Graaf et al.

    Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco

    Plant Cell

    (2005)
  • M.L. Preuss et al.

    A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana

    J Cell Biol

    (2006)
  • M.L. Preuss et al.

    The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells

    Plant Cell

    (2004)
  • U. Fischer et al.

    Lipid function in plant cell polarity

    Curr Opin Plant Biol

    (2004)
  • D. Monteiro et al.

    Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion

    J Exp Bot

    (2005)
  • P. Vincent et al.

    A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs

    J Cell Biol

    (2005)
  • S.E. Phillips et al.

    The diverse biological functions of phosphatidylinositol transfer proteins in eukaryotes

    Crit Rev Biochem Mol Biol

    (2006)
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