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Cell Biology International (2007) 31, 649–654 (Printed in Great Britain)
Involvement of the cytoskeleton in the secretory pathway and plasma membrane organisation of higher plant cells
Yohann Bouttéa1, Samantha Vernhettesb and Béatrice Satiat‑Jeunemaitrea*
aLaboratoire de Dynamique de la Compartimentation Cellulaire, Institut des Sciences du Végétal, CNRS UPR2355, Båtiment 23/24, Avenue de la Terrasse, 91198 Gif-sur-Yvette cedex, France
bLaboratoire de Biologie Cellulaire Jean-Pierre Bourgin Institute, INRA, Route de Saint-Cyr, 78026 Versailles, France



Keywords: Endomembranes, Cytoskeleton, Golgi apparatus, Plasma membrane, Regulated exocytosis, Microscopy.

1Present address: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, SE-901 83 Umeå, Sweden.

*Corresponding author. Tel.: +33 1 6982 3798; fax: +33 1 6982 3355.


1 The cytoskeleton and the ER-GA complex

1.1 Structural and dynamic organisation

Most endomembrane and cytoskeleton interrelationships were first investigated through pharmacological approaches. The effects of cytoskeleton inhibitors (mostly oryzalin/colchicine for microtubules, cytochalasin D/latrunculin B for actin) on endomembrane organisation and function were investigated in various plant cell models. Three main parameters were usually considered: effects of cytoskeleton inhibitors on compartment morphology, dynamics, and 3D organisation. It became rapidly clear that neither actin nor microtubules were directly controlling the specific shape of ER tubules or Golgi stacks. On the other hand, and in contrast to their yeast or animal counterparts, plant endomembrane organisation strongly depends on actin filaments (Satiat-Jeunemaitre et al., 1996; Boevink et al., 1998; Nebenführ et al., 1999; Brandizzi et al., 2002; Tamura et al., 2005). Bio-imaging techniques have revealed for a long time that the 3D organisation of ER was actin dependent (Knebel et al., 1990). However, in some cases a clear distinction is made between a sub-cortical ER tubules which moves on actin bundles, and a cortical ER with fine meshes largely independent of cytoskeleton (I. Foissner, personal communication).

Light and electron microscopy studies have also suggested that the depolymerisation of actin provokes a clear disruption of the GA, Golgi stacks piling up in small aggregates in the cells (Satiat-Jeunemaitre et al., 1996). The more recent in vivo imaging techniques have confirmed this actin-dependent organisation and have further revealed that individual Golgi stacks were closely associated with specific sites on the surface of the cortical ER, moving together on the ER surface (daSilva et al., 2004; Yang et al., 2005). This ER network itself, overlies an actin filament network and in absence of actin, Golgi stacks were actually piling up around the ER branching points forming the specific cytochalasin-induced aggregates previously mentioned (Boevink et al., 1998; Brandizzi et al., 2003). Thirdly, the actin cytoskeleton is also responsible for the movements of both ER tubules and individual Golgi stacks, as cytochalasin/latrunculin blocks the motility of both elements. The GA may interact with actin via the proteins Kam1/MUR3 which is Golgi localised (Tamura et al., 2005).

1.2 Functional organisation: The cytoskeleton is not directly involved in cargo exchanges between ER and GA

Macromolecule exchanges between ER and GA and possibly from GA to ER are associated with a complex molecular machinery. The involvement of the cytoskeleton and its related protein machineries is expected in such processes, in relation with the common view that transport from one compartment to the other is vesicle dependent. That is the case in most of the mammalian cells. However in plant cells, such cytoskeleton dependency has never been shown. Brandizzi et al. (2002) have actually shown that transport of cargo molecules from ER to GA is not dependent on the movement of Golgi stacks on ER tracks, and is cytoskeleton independent (Saint-Jore et al., 2002). Nevertheless, this ER-GA pathway is energy dependent. Alternative hypotheses to the vesicle shuttle such as the transient membrane continuum between the two compartments has been proposed (Hawes and Satiat-Jeunemaitre, 2005; Moreau et al., 2006).

2 In interphase cells, GA to plasma membrane transport is mainly actin-dependent

Far from being static, localisation and function of plasma membrane proteins and lipids are regulated throughout both secretory and recycling/endocytic pathways. A comprehensive view of plant plasma membrane protein and lipid localisation should therefore integrate knowledge on secretory and endocytic pathways together with the cytoskeletal requirement of these pathways.

In polarized epithelial cells in animals, microtubules are deposited longitudinally along the apical-basolateral axis. This spatial organisation forms tracks which are used by post-Golgi secretory vesicles and the endocytic apparatus to ensure the delivery of proteins to specific surface domains (Toomre et al., 1999; Kreitzer et al., 2003; Musch, 2004). In plant cells, although the exact requirement of cytoskeleton in such processes is far from established, actin rather than microtubules appears to play the essential function in material delivery to the cell surface in polarised and non-polarised cells. It is indeed well documented that actin filaments are responsible for the transport of secretory vesicles away from the Golgi stacks, as actin depolymerisation induces an accumulation of Golgi derived vesicles in the periphery of the Golgi stack.

Moreover, in tip of growing cells like pollen tubes, root hairs or trichoblasts, the role of actin filaments as tracks carrying secretory vesicles derived from the GA to the growing tip has been well established (Mathur, 2004; Vidali et al., 2001; Picton and Steer, 1981). Similarly, polysaccharides and enzymes involved in cell wall morphogenesis also require an intact actin network to be properly secreted from the GA to the cell wall (Blancaflor, 2002; Hu et al., 2003). This movement is myosin dependent (Miller et al., 1995; Satiat-Jeunemaitre et al., 1996; Nebenführ et al., 1999). Note that so far, only myosin VIII, XI and XIII are presents in plants (http://www.mrc-lmb.cam.ac.uk/myosin/myosin.html). Actin may also play essential function regarding the post-Golgi trafficking events to the vacuoles. It is well established that plant vacuoles have a highly dynamic structure, and part of their 3D organisation also appears to be actin-dependent (Uemura et al., 2002; Saito et al., 2002).

Some reports have however shown that some actin independent exocytosis of membrane protein: in leaf protoplasts, the delivery of H+-ATPase:GFP and invertase:GFP to the plasma membrane appears to be independent from an intact actin network (Kim et al., 2005). This protoplast model may reveal some specific actin-independent pathways which are more active in protoplasts than under normal physiological conditions.

3 Retrograde pathways from plasma membrane: actin-dependent?

The recent data on the dynamics of the PIN protein family kindles the debate on the occurrence of specific recycling/endocytic pathways in the cortical cytoplasm beneath the plasma membrane and its specific cytoskeleton requirements. PIN proteins are integral membrane proteins which facilitate auxin transport out of the cell. They are usually localised on one side of the growing cell, canalising the auxin efflux to a neighbour cell. They also label some intracellular components of the endomembrane system, like Golgi stacks or more frequently endosome-like structures (Boutté et al., 2006). As for the GA and other subcellular organelles, the motility and the 3D organisation of the PIN-labelled compartments are actin dependent. In maize root cells, it has been shown that, even in absence of actin, the PIN proteins may still be retrieved from plasma membrane in the presence of Brefeldin A treatment (BFA, a drug known to block exocytic but not endocytic events).

This observation suggests that actin was not involved in this PIN retrograde pathway from plasma membrane to endosomes (Boutté et al., 2006). However, the transport back to the plasma membrane of these recycled proteins seems to be actin dependent (Geldner et al., 2003). This was also true for other protein candidates for recycling like the GNOM proteins (an ARF exchange actor) in Arabidopsis thaliana root cells (Geldner et al., 2001, 2003). Therefore a strict actin dependency of retrograde movements from plasma membrane has not been directly demonstrated so far. Examples from characean cells suggest that actually two pathways may coexist, presenting the different dependency of actin: one constitutive endocytic pathway would be actin independent meanwhile a wound-induced endocytic processes would be actin-dependent (Foissner and Klima, in press).

Cytoskeleton dependent trafficking events have also been described for some lipid components. In animal cells, biosynthetic cholesterol trafficking from the ER to the GA and up to the plasma membrane is a microtubule dependent pathway (Heino et al., 2000). In plant cells the cytoskeleton requirement in the sterol biosynthetic transport form ER to the plasma membrane is not known (Moreau et al., 1998). However, Grebe et al. have shown that in Arabidopsis thaliana root cells, actin cytoskeleton was involved in sterol trafficking events from plasma membrane to endosome-like compartments labelled with ARA6, a Rab5GTPase homologue (Grebe et al., 2003).

4 Microtubule requirement in membrane trafficking and cell surface organisation

From the examples described above, endomembrane trafficking events in growing cells seem to restrict the cytoskeleton requirements to the actin network. The depolymerisation of microtubules had no or indeed little effect on 3D organisation, motility and function of the endomembrane system. The main function of microtubules in plant cells have been assigned to the control of cell wall morphogenesis, by direct or indirect effects on the positioning of cell wall microfibrils. However recent studies on the mechanisms of cell wall morphogenesis and cell polarity outline a potential role for microtubules in controlling some trafficking events underneath the plasma membrane.

The first set of data concerns the effects of microtubule depolymerisation on the localisation of PIN proteins. In Arabidopsis thaliana and Zea mays root cells, it was shown that after 24h of microtubule disruption, some PIN proteins, usually solely localised on the basal membrane of cells, are relocalised to the inner lateral membrane (Boutté et al., 2006). Therefore in the absence of microtubules, the cell still has the ability to organise the PIN proteins in specific macrodomains but has lost the right positional information to decide where to place them. This reorientation of the polar axis at the plasma membrane upon long term oryzalin treatment is similar to the reorientation of the growth symmetry in defective-microtubules organisation mutants like tonneau (ton). In ton2 mutant, PIN proteins are still localised in a polar manner within the cells, however the tissue organisation is chaotic as if some positional information is missing (Boutté et al., 2006).

The interrelations between the occurrence of microtubule defects and the loss of anisotropic growth have been reported for other microtubule-defective mutants like bot1/fra2 or mor1, where growth symmetry was changed (Camilleri et al., 2002; Bichet et al., 2001; Burk and Ye, 2002; Whittington et al., 2001). In these mutants root cell growth is largely isotropic instead of anisotropic. The growth anisotropy is thought to be controlled by cellulose microfibril orientation (Taiz, 1984; Scheible et al., 2003; Williamson et al., 2001; Lane et al., 2001), and cellulose orientation may be guided by cortical microtubules (Giddings and Staehelin, 1991; Baskin, 2001; Sugimoto et al., 2003). This “syndrome” microtubule/microfibrils is however still not clear after more than 20years of debate (see Paradez et al., 2006 for review).

The recent data on the proteins possibly involved in cell wall morphogenesis and their requirement for microtubules bring new insight in this question. For example, one mutant exhibiting a growth symmetry defect is the cobra mutant which is defective in the GPI-anchored protein COBRA. This mutant is characterized by a loss of anisotropic expansion and consistently, a disorganisation of cellulose microfibril orientation (Roudier et al., 2005). The COBRA protein is localised to plasma membrane macrodomains (mostly longitudinal) in a microtubule-dependent mechanism (Roudier et al., 2005), reinforcing the concept of a specific orchestration in the cell cortex between microtubules, membrane trafficking and cell wall organisation. A striking argument in favour of this is provided by the example of the protein Korrigan (KOR1), an endo-1,4-β-d-glucanase, involved in cellulose synthesis (Molhoj et al., 2001; Nicol et al., 1998).

It was shown that KOR1 is localized in two compartments, i.e. the GA and mostly an endosome-like population (Robert et al., 2005). The motility of this heterogeneous population is both actin and microtubule dependent. A sub-population of KOR1 endomembrane compartments follows linear trajectories along the plasma membrane. The microtubule-disorganisation drug oryzalin abolished this motility (Robert et al., 2005). Similarly to the KOR1 example, it has been shown that one protein from a cellulose synthase complex: CESA6, is positioned into the plasma membrane by a functional association with microtubules (Paredez et al., 2006). The fluorescent version of CESA6 allows observation of colinearity between the movement of CESA6 and the orientation of cortical microtubules that is also conserved when microtubules are reoriented. Interestingly, complete removal of microtubules upon longer treatments with oryzalin did not abolish the linear movement of the particles.

Vernhettes and collaborators proposed that microtubules may be involved in the regulation of an endosomal population loaded with cell wall machinery enzymes (Robert et al., 2005). This regulatory activity could concern movements and unloading, of these compartments, comparable to processes described for regulated exocytotic or recycling pathways in animal cells and may be highly dependent of the physiological stages of the cells. The delivery of KOR1 to the plasma membrane in proximity to cellulose synthase complexes may for instance facilitate the clearance of the complexes from the membrane. As mentioned above, the GPI-anchored COB protein may also play a role in the interaction between cellulose synthase complexes and microtubules, for instance by controlling the microtubule-dependent movement of the complexes.

5 Concluding remarks

Cytoskeleton requirements in anterograde or retrograde transport within cells differ between animals and plants, being mainly actin-based in plant and microtubule-based in animal and also in yeast cells. However, the exact involvement of actin in endocytic processes has yet to be further investigated. One may note that these statements have to be considered in respect to the position of the plant cell into the cell cycle. Indeed, during cell division, plants establish a different system to the one used for the trafficking from the GA to the plasma membrane during interphase. It has been shown that directed transport of vesicles to the division plan is ensured by phragmoplast microtubules via kinesin-like proteins (Otegui et al., 2001; Segui-Simarro et al., 2004, see Jürgens, 2005 for review).

On the other hand, in plant cells the early steps of macromolecular transport from ER to GA appears cytoskeleton independent, challenging the classical view of a vesicular shuttle between the two organelles. Finally, microtubules seem to have a role to play in the cortical zone beneath the plasma membrane, either in the detection of positional information, or in the regulation of the dynamics of endosomal/recycling compartments. Such microtubule-dependent motility has actually been observed for mitochondria and cortical ER dynamics in early stage of elongation of characean internodal cells (Foissner, 2004).

They would be associated with a zone of high regulation for secretory/recycling activity. The recent discovery of a new member AtEXO70A1 of a family of putative exocyst subunits (a multimeric complex involved in spatially regulated exocytosis in yeast and animal cells), involved in cell and organ morphogenesis (Synek et al., 2006), reinforces the view that some plant exocytotic processes may indeed be far more regulated than previously thought.

Acknowledgements

Thanks are due to Ilse Foissner (University of Salzburg, Austria) for discussion on characean green algae and for her constructive comments on this manuscript.

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Received 5 November 2006/12 December 2006; accepted 10 January 2007

doi:10.1016/j.cellbi.2007.01.006


ISSN Print: 1065-6995
ISSN Electronic: 1095-8355
Published by Portland Press Limited on behalf of the International Federation for Cell Biology (IFCB)