The Rho/Rop small GTPase regulatory module is central for initiating exocytotically ACDs (active cortical domains) in plant cell cortex, and a growing array of Rop regulators and effectors are being discovered in plants. Structural membrane phospholipids are important constituents of cells as well as signals, and phospholipid-modifying enzymes are well known effectors of small GTPases. We have shown that PLDs (phospholipases D) and their product, PA (phosphatidic acid), belong to the regulators of the secretory pathway in plants. We have also shown that specific NOXs (NADPH oxidases) producing ROS (reactive oxygen species) are involved in cell growth as exemplified by pollen tubes and root hairs. Most plant cells exhibit several distinct plasma membrane domains (ACDs), established and maintained by endocytosis/exocytosis-driven membrane protein recycling. We proposed recently the concept of a ‘recycling domain’ (RD), uniting the ACD and the connected endosomal recycling compartment (endosome), as a dynamic spatiotemporal entity. We have described a putative GTPase–effector complex exocyst involved in exocytic vesicle tethering in plants. Owing to the multiplicity of its Exo70 subunits, this complex, along with many RabA GTPases (putative recycling endosome organizers), may belong to core regulators of RD organization in plants.

Introduction

Plant cell morphogenesis relies upon a dynamic network of processes integrating cell wall dynamics with signal transduction, changes in ion membrane transports, membrane lipid modifications, regulation of the secretory pathway and cytoskeleton dynamics. In the present review, we will separate and focus on Rab and especially Rop GTPase-regulated processes because of the importance of, especially, Rops in plant cell and tissue morphogenesis [14].

Non-covalent binding of GTP to small GTPase proteins imposes conformational changes on these proteins: GTPases are ideal molecular switches for regulatory and signal transduction pathways. Low intrinsic GTPase activity allows a relatively long life time for their active, GTP-bound, conformation and the intervention of a GAP (GTPase-activating protein) switches off the GTPase to the inactive, GDP-bound, state.

Most small GTPases are post-translationally modified at their C-termini, but sometimes also at their N-termini by addition of hydrophobic farnesyl, geranylgeranyl or acyl moieties, making them peripheral membrane proteins that cycle between membranes (often sequestered into membrane rafts) and cytoplasm [2]. This cycling is regulated by GDIs (GDP-dissociation inhibitors), which are thought to extract GDP-bound GTPases from the target membranes for possible recycling through GDP–GTP exchange and reactivation. Such exchange is catalysed by GEFs (guanine-nucleotide-exchange factors) [3]. Small Rab and Rho/Rop GTPases are able to organize specific membrane domains, helping to initiate and maintain vectorial/targeted processes of cell morphogenesis and signalling within the cell [26]. Collectively, they are implied in the regulation of the secretory pathway (e.g. the identity of endomembrane compartments, formation, transport, docking and fusion of vesicles with the target membrane and membrane recycling), actin cytoskeleton dynamics, cell wall synthesis, activity of membrane-bound enzymes and transporters (e.g. membrane lipid-modifying enzymes and NADPH oxidases). We focus here exclusively on the plant effectors of Rab and Rop GTPases as their regulators have been described in detail previously [25].

Rab GTPases

Rab GTPases of land plants are divided into subgroups homologous with animal and fungal ones, yet they have diverged structurally and functionally so that obvious plant specific features are discernible [4,5,7]. It is interesting that we know much about plant Rab regulators, but very little about plant Rab effector proteins [4], in contrast with the situation in Opisthokonts. In fact, the only ones well characterized are two membrane phospholipid-modifying Arabidopsis phosphatidylinositol 4-kinases: AtPI4Kβ1 and AtPI4Kβ2. Both interact with RabA4b, a GTPase controlling post-Golgi to PM (plasma membrane) trafficking in root hair tips [5]. A double mutant lacking both genes exhibits reduced exocytotic vesicle formation, resulting in enlarged vacuoles and aberrant root hair growth [9]. It was proposed that this type of Rab effector might play a prominent role in the organization of endomembrane trafficking, including exocytic membrane containers [10,11]. In yeast, the exocytic/secretory vesicle-tethering complex exocyst [which mediates vesicle docking to PM before SNARE (soluble N-ethylmaleimide-sensitive factor-attachment protein receptor) fusogenic complex assembly] was first discovered as an effector of Sec4 Rab GTPase [12] and that is why, in our laboratory, we are looking into the possible interaction of the plant exocyst with plant Rab GTPases ([8], and H. Toupalová, M. Hála and V. Žárský, unpublished work). Later, many more interactions of the exocyst with Rho/Rac GTPase were discovered in yeast and animals (see below). Obviously, the search for plant Rab GTPase effectors is an urgent task and a necessity for the future understanding of the plant secretory pathway regulation. Owing to specificities in the plant Rab family, it is expected that the effector repertoire of plant Rabs will be partly distinct from what is known in yeast and mammals [4,5,10].

Rop GTPases

The Rop group of plant-specific Rho GTPases diverged from the closely related Rac GTPases and the specificity of plant Rop GTPases is demonstrated by the discovery of new specific group of PRONE (plant-specific Rop nucleotide exchanger) GEFs, which are absent from animals and fungi [13,14]. For the establishment of ACDs (active cortical domains) on the PM of plant cells, it is crucial that these PRONE GEFs are activated by serine/threonine RLKs (receptor-like kinases) which represent a very diverse group of plant-specific proteins involved in all aspects of plant signal transduction and development [15].

There are two major subfamilies within the Rop family, each with distinct features, localization mechanisms and possible functions. Subfamily I Rops (represented in Arabidopsis by ROP1–ROP8) contain the conventional C-terminal motif (present in the majority of non-plant Rho GTPases) for prenylation. Subfamily II Rops (represented in Arabidopsis by ROP9–ROP11) are not prenylated, but are rather palmitoylated at a cysteine-containing motif that appears to be a plant-specific innovation [2].

Localization of Rops to the PM is dependent on the C-terminal hydrophobic modifications; surprisingly, the type I Rop GTPases are also transiently acylated by palmitic and stearic acid when in the active, GTP-bound, conformation. This modification stabilizes their membrane localization and induces partitioning into DRMs (detergent-resistant membranes), also called lipid rafts [2].

Rop effectors

RICs [Rop-interacting CRIB (Cdc42/Racinteracting binding domain) motif-containing proteins], Arp2/3 (actin-related protein 2/3) complex and actin

It is well established that the highly dynamic fine F-actin (filamentous actin) cytoskeleton meshwork is important in all plant cell morphogenetic processes. Rop GTPases are crucial for proper actin organization in plants, as exemplified in root hairs and in pollen tubes [16,17], at least in part via plant-specific RICs as downstream effectors of Rop GTPases [18,19]. RICs are the first plant Rop effectors to be described; they are small proteins, comprising 11 members of diverse sequence in Arabidopsis thaliana that contain no recognizable features other than the CRIB domain [18]. Specifically, RIC4 regulates actin at the pollen tube tip, whereas RIC3 provides counteracting regulation of the tip-high Ca2+ gradient (Table 1).

Table 1
Rop effector proteins

CCR1, cinnamoyl-CoA reductase 1; MAPK, mitogen-activated protein kinase; NCRK, novel cysteine-rich kinase; RBK, Rop-binding protein kinase; RLCK, receptor-like cytoplasmic kinase; RRK, Rop-interacting receptor-like kinase; UGT, UDP-glucose transferase.

Rop effector Function Reference 
RIC1 Microtubular dynamics [18
RIC3 [Ca2+]i/actin dynamics [52
RIC4 Actin dynamics [52
PIP5K* PtdIns(4,5)P2 synthesis [34
PIR-SCAR/WAVE Arp2/3/actin dynamics [53
NOX ROS production/signalling [21
ICR1 Sec3/exocyst, exocytosis [44
UGT Callose synthesis [54
CCR1 Lignification/innate immunity [55
MAPK* MAPK signal transduction [56
PLD* Membrane lipid signalling [57
RACK1A–RAR1 complex Rice innate immunity [24
NCRK Xylem development [58
RBK2–RLCK Pollen or xylem development [58
RBK1–RLCK Innate immunity [58
RRK1/RRK2–RLCK RLCK activation mechanism [59
*Direct interaction not proven. For an overview of predicted Arabidopsis 
Rop effectors, see [60]. 
Rop effector Function Reference 
RIC1 Microtubular dynamics [18
RIC3 [Ca2+]i/actin dynamics [52
RIC4 Actin dynamics [52
PIP5K* PtdIns(4,5)P2 synthesis [34
PIR-SCAR/WAVE Arp2/3/actin dynamics [53
NOX ROS production/signalling [21
ICR1 Sec3/exocyst, exocytosis [44
UGT Callose synthesis [54
CCR1 Lignification/innate immunity [55
MAPK* MAPK signal transduction [56
PLD* Membrane lipid signalling [57
RACK1A–RAR1 complex Rice innate immunity [24
NCRK Xylem development [58
RBK2–RLCK Pollen or xylem development [58
RBK1–RLCK Innate immunity [58
RRK1/RRK2–RLCK RLCK activation mechanism [59
*Direct interaction not proven. For an overview of predicted Arabidopsis 
Rop effectors, see [60]. 

Analysis of ‘distorted’-type trichome mutants in A. thaliana indicates that the Arp2/3 complex, which provides branched actin nucleation activity, is required for wild-type cell morphogenesis in some plant cell types (reviewed in [19]). Furthermore, Arp2/3 activity is regulated by the SCAR (suppressor of cAMP receptor)/WAVE [WASP (Wiskott–Aldrich syndrome protein) verprolin homologous] complex, which appears to contain SPIKE1, first uncovered as a plant Rop GEF, as well as SCAR proteins that are direct targets of activated Rops [20] (Table 1).

NOXs (NADPH oxidases), RACK1A (receptor for activated C-kinase 1A)–RAR1 (required for Mla12 resistance 1) complex, phosphoinositide kinases and phospholipases in polar growth and defence

In metazoan cells, Rho exerts its function through multiple cross-regulatory pathways that also involve lipid and ROS (reactive oxygen species) signalling. Similarly, recent reports have shown that Rop function in plant cells depends on multiple feedback regulatory mechanisms, which may control the activity of both Rops themselves and their regulators and effectors [2].

NOXs belong among the best-characterized effectors of Rac GTPases in animal cells, and the same is true in plants [21] (Table 1). In mammals, Rho GTPase is a well-described activator of the phagocyte NOX. Recently, a functional Rop–NOX interaction was demonstrated, as the rice Rop homologue OsRac1 was shown to bind and activate RbohB through its EF-hand-containing N-terminal part [21] (Figure 1). Activated Rop stimulates NOX activity and ROS production in root hairs, but also during plant–pathogen interaction and leaf development [22,23]. Recently, Rop-regulated RACK1A–RAR1 complex [including Rop-interacting HSP90 (heat-shock protein 90)] was discovered to be active in rice innate immunity [24] (Table 1) and both ROS formation during disease resistance [22] and ROS-mediated cell death [25] are dependent on the Rac/Rop OsRac1. Similarly in dicotyledons, active GTP-bound ROP2 activates superoxide production in vitro [23]. Because plant NOX proteins are endowed with two Ca2+-binding EF-hands at their N-terminus (and also are activated by phosphorylation), they are integrated into formation of the tip-high Ca2+ gradient in polar growing cells by the stimulation of ROS-activated Ca2+-influx channels [26].

Model depicting the central role of activated Rop and its effectors in the regulation of cell polarity in plants

Figure 1
Model depicting the central role of activated Rop and its effectors in the regulation of cell polarity in plants

Arrows indicate positive regulation, broken arrow indicates regulation mode that has not been proved yet in plant cells. MAPK, mitogenactivated protein kinase; PI4P-5K, phosphatidylinositol 4-phosphate 5-kinase; PIR, PIROGI, WAVE complex subunit SRA1 homologue.

Figure 1
Model depicting the central role of activated Rop and its effectors in the regulation of cell polarity in plants

Arrows indicate positive regulation, broken arrow indicates regulation mode that has not been proved yet in plant cells. MAPK, mitogenactivated protein kinase; PI4P-5K, phosphatidylinositol 4-phosphate 5-kinase; PIR, PIROGI, WAVE complex subunit SRA1 homologue.

Lipid signalling pathways have also been implicated in NOX regulation. Phosphatidylinositol 3-kinase and PLD (phospholipase D) produce PtdIns3P and PA (phosphatidic acid) respectively, providing phospholipids to which metazoan regulatory subunits p47phox and p40phox bind. PA has also been shown to activate neutrophile NOX in cell-free systems [27]. Interestingly, ROS (particularly H2O2) activate PLD [28], suggesting possible feedback regulation. Significantly, phospholipid second messengers are also involved in ROS signalling in plant cells. PA treatment stimulates ROS production in Arabidopsis leaves [23,29] and PLD–PA tandem is involved in promoting the elicitor-induced generation of ROS [30] (Figure 1).

Involvement of possibly indirect Rop effector PLD (although in animals PLD activity is regulated directly by Rho) in plant cell morphogenesis was implied by the ectopic expression of PLDζ1 (and presumably concomitant generation of its product PA), which resulted in the initiation of ectopic root hairs [31]. We have shown that PLD-derived PA stimulates cell expansion in pollen tubes [32]; as PA was shown to co-activate Rop-mediated ROS production in a cell death response [23], we speculate that PA derived from PLD might similarly co-activate Rop-mediated ROS production (e.g. through NOX) during formation of ACDs (Figure 1). Arabidopsis PLDα1 has been implicated in increasing NOX activity and ROS production [29] and PLDα1-produced PA interacts directly with the N-terminal domain of NOX isoform RbohD in guard cells. This interaction elevates RbohD activity needed for ABA (abscisic acid)-mediated ROS production and stomatal closure [33].

As in animals, Rop might stimulate PLD and PLC activity via PtdIns(4,5)P2 synthesis by the activation of PIP5K (phosphatidylinositol 4-phosphate 5-kinase) [34] (Table 1), which may also be stimulated by PA [35]. Detailed mechanistic role of Rop-stimulated PA production in cell polarity is still largely unknown, although several scenarios can be drawn from non-plant organisms [11]. Reciprocal stimulation of PLD and PIP5K has been hypothesized to generate rapid feed-forward loops for localized and explosive generation of PA and PtdIns(4,5)P2, which may then govern the recruitment and activation of proteins to a membrane domain to execute specific tasks, e.g. membrane trafficking and actin dynamics (reviewed in [36]) (Figure 1). The very tip of growing root hairs and pollen tubes could be such a domain, as PM in this region is PtdIns(4,5)P2-enriched [34,37]; type I Rops show similar localization patterns (reviewed in [38]). Thus known mechanisms in plant cells are capable of building a specific PM domain based on reciprocal activation of PIP5K, PLD–PA and Rop activities. As NOX-produced ROS are able to stimulate Ca2+ influx and Ca2+ is able to stimulate NOX activity, it is reasonable to assume a contribution of this positive-feedback mechanism to the creation of the tip-high Ca2+ gradient [26,39]. We hypothesize that both of these positive-feedback loops might contribute to the definition of specific ACDs (Figures 1 and 2).

Schematic representation of the RD concept

Figure 2
Schematic representation of the RD concept

Arrows indicate endo- and exo-cytic membrane trafficking between PM domains and corresponding recycling endosomes (RE) respectively. See the text and [11] for details.

Figure 2
Schematic representation of the RD concept

Arrows indicate endo- and exo-cytic membrane trafficking between PM domains and corresponding recycling endosomes (RE) respectively. See the text and [11] for details.

ICR1 (interactor of constitutive active Rops 1): link from active Rops to the exocyst complex and exocytosis

The exocyst is an octameric effector complex of both Rho and Rab GTPases, integrating signals at the final stages of polarized secretory pathways and functioning as exocytotic vesicles to the PM-tethering complex in yeast and animal cells [40]. We have accumulated evidence that the exocyst is active in the regulation of plant cell morphogenesis as well [8,4143]. The first link from GTP-charged Rop to the Sec3a subunit of the plant exocyst was uncovered recently via the scaffold protein ICR1 [44], in contrast with the situation in fungi and animals where Rho interacts directly with Sec3 (reviewed in [40]). The function of the exocyst, although originally related almost exclusively to exocytosis, is now also established in membrane recycling via recycling endosomes in collaboration with Rab11 [45].

Recycling domains

Intriguingly, localized exocytosis, coupled with endocytosis and recycling, is a mechanism for maintaining dynamic polarization of membrane proteins, if diffusion to equilibrium distribution in the membrane is slow [46]. Such domains of localized exocytosis/rapid recycling may be found in plant cells [4749]. Given that overexpression of an activated type II Rop (CA-ROP11) blocks endocytosis in Arabidopsis root hairs [50], it seems likely that Rops will also be involved in the regulation of membrane recycling. As mentioned above, in animal cells, the exocyst-interacting Rab11 GTPase is a known regulator of membrane recycling, and there is strong evidence for participation of the Rab11–exocyst module in membrane recycling [45]. Plant cells in situ mostly have more PM surface/cell wall domains and are many-sided {Figure 2; examples are different PINs (auxin efflux carriers) or polarization/localization PM domains [49] or as a visible product, such as cell wall domains around, e.g., epidermal cells} and we have recently proposed that the initiation and maintenance of different PM surfaces within the same plant cell might be connected to the associated membrane proteins recycling via specific endosomes. Surface domains (primarily at the PM, but which have an impact on the cell wall, the ACDs) are connected by membrane recycling via recycling endosomes into the spatiotemporal units called RDs (recycling domains) [11]. Multiplicity of RabA/Rab11, and possibly some other Rab paralogues, in plant cells is able to support the coexistence of different recycling compartments/endosomes within the same plant cell [7,51], whereas multiplicity and co-expression of different exocyst PM-targeting Exo70 subunits in the same plant cells allows several different ACDs (landmark domains) on the PM surface of the same cell [8,11,43]. A search for and studies of Rab and Rop effectors should substantially facilitate the analysis and understanding of localization/recycling pathways of plant membrane proteins and cell wall differentiation.

Experimental Plant Biology: Why Not?!: 4th Conference of Polish Society of Experimental Plant Biology, an Independent Meeting held at Jagiellonian University, Krakow, Poland, 21–25 September 2009. Organized and Edited by Kazimierz Strzałka (Jagiellonian University, Krakow, Poland).

Abbreviations

     
  • ACD

    active cortical domain

  •  
  • Arp2/3

    actin-related protein 2/3

  •  
  • CRIB

    Cdc42/Rac-interacting binding domain

  •  
  • GEF

    guanine-nucleotide-exchange factor

  •  
  • ICR1

    interactor of constitutive active Rops 1

  •  
  • NOX

    NADPH oxidase

  •  
  • PA

    phosphatidic acid

  •  
  • PIP5K

    phosphatidylinositol 4-phosphate 5-kinase

  •  
  • PLD

    phospholipase D

  •  
  • PM

    plasma membrane

  •  
  • PRONE

    plant-specific Rop nucleotide exchanger

  •  
  • RACK1A

    receptor for activated C-kinase 1A

  •  
  • RAR1

    required for Mla2 resistance 1

  •  
  • RD

    recycling domain

  •  
  • RIC

    Rop-interacting CRIB motif-containing protein

  •  
  • ROS

    reactive oxygen species

  •  
  • SCAR

    suppressor of cAMP receptor

  •  
  • WAVE

    WASP (Wiskott–Aldrich syndrome protein) verprolin homologous

We apologize to many colleagues whose work cannot be mentioned here because of space limitations.

Funding

The work on these topics is supported by the Academy of Sciences of the Czech Republic Grant Agency [grant number IAA601110916 (to V.Ž.)], The Czech Science Foundation [grant number 522/09/P299 (to M.P.)] and the Czech Ministry of Education, Youth and Sports [grant numbers LC06034-REMOROST, MSM 0021620858 and KONTAKT MSMT CR ME10033 (to V.Ž.)].

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