- Email: [email protected]
Plant Cytokinesis: Terminology for Structures and Processes
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Opinion
Plant Cytokinesis: Terminology for Structures and Processes Andrei Smertenko,1,* Farhah Assaad,2 František Baluška,3 Magdalena Bezanilla,4,23 Henrik Buschmann,5 Georgia Drakakaki,6 Marie-Theres Hauser,7 Marcel Janson,8 Yoshinobu Mineyuki,9 Ian Moore,10 Sabine Müller,11 Takashi Murata,12 Marisa S. Otegui,13 Emmanuel Panteris,14 Carolyn Rasmussen,15 Anne-Catherine Schmit,16 Jozef Šamaj,17 Lacey Samuels,18 L. Andrew Staehelin,19 Daniel Van Damme,20,21 Geoffrey Wasteneys,18 and Viktor Žárský22 Plant cytokinesis is orchestrated by a specialized structure, the phragmoplast. The phragmoplast first occurred in representatives of Charophyte algae and then became the main division apparatus in land plants. Major cellular activities, including cytoskeletal dynamics, vesicle trafficking, membrane assembly, and cell wall biosynthesis, cooperate in the phragmoplast under the guidance of a complex signaling network. Furthermore, the phragmoplast combines plant-specific features with the conserved cytokinetic processes of animals, fungi, and protists. As such, the phragmoplast represents a useful system for understanding both plant cell dynamics and the evolution of cytokinesis. We recognize that future research and knowledge transfer into other fields would benefit from standardized terminology. Here, we propose such a lexicon of terminology for specific structures and processes associated with plant cytokinesis.
Trends A large number of phragmoplast proteins have been identified. Electron microscopy/tomography studies have produced nanoscale information about the architecture of phragmoplast and cell plate assembly stages in cryofixed cells. Novel components of the cortical division zone and cell plate fusion site have been discovered. This information lays a foundation for understanding how plant cells memorize the division plane throughout mitosis and how the cell plate is guided to its predetermined attachment site.
Rationale for Updating Plant Cytokinesis Terminology Current plant cytokinesis terminology was developed using data generated by fluorescence microscopy of live or fixed cells, electron microscopy of chemically or cryofixed cells, and genetic strategies. As a consequence of different experimental approaches, and for historic reasons, the cytokinetic processes and structures are often referred to by different names. Because plant cytokinesis has become a useful model system for addressing specific questions in plant biochemistry, cell biology, development, etc., we recognize that exchange of information between scientists working in these diverse fields, as well as further advancement of plant cytokinesis research, would benefit from a harmonized terminology. Here, we summarize the steps[376_TD$IF], and update terminology associated with two major processes in plant cytokinesis: determination of the cell division plane and assembly of the cell plate (Table 1). We also propose established markers for some processes and structures (Table 2). The terminology proposed here uses cytokinesis in somatic cells as an example and takes advantage of available structural information. Division in reproductive organs and specialized cell types involves similar processes, which appear to be structurally different [1]. For in-depth description of cytokinesis in somatic cells we refer to several recent reviews [2–6]. Terminology
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MAP65 and plus end-directed kinesins contribute to the maintenance of the antiparallel overlap of phragmoplast microtubules. In addition, the MAP65–TRAPPII interaction plays a key role in cell plate assembly. Actin filaments align parallel to microtubules in the phragmoplast, while some microfilaments extend from cell plate margin to guide its expansion towards the fusion site.
1
Institute of Biological Chemistry, Washington State University, Pullman, WA 99164, USA 2 Botany Department, WZW, Technische Universität München, Freising, 85354 Germany
http://dx.doi.org/10.1016/j.tcb.2017.08.008 © 2017 Elsevier Ltd. All rights reserved.
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Table 1. Glossary of [374_TD$IF]Plant Cytokinesis Terminology Term
Former terms
Description Cortical region of cytoplasm with few actin filaments that forms prior to nuclear envelope breakdown and usually coincides with the cortical division zone (CDZ). ADZ can be flanked by domains enriched in actin filaments, known as a twin-peaks structure in some cell types.
Actin-depleted zone (ADZ)
Cell division plane
Anticipated or true position of the cell plate.
Cell plate
Membrane-polysaccharide compartment that partitions the cytoplasm after nuclear division.
Cell plate assembly
General term referring to all processes from cell plate biogenesis to maturation.
Cell plate assembly matrix (CPAM)
Amorphous scaffold system consisting of proteins and vesicles in the phragmoplast midzone (150 nm thick) that is responsible for mobilization of protein complexes and vesicles involved in cell plate assembly.
Cell plate attachment
Process of cell plate anchoring and fusion to the parental plasma membrane and cell wall.
Cell plate biogenesis
Generation of a membrane compartment via vesicle tethering and fusion inside the CPAM. Transport protein particle (TRAPP)II is the predominant tethering complex.
Cell plate expansion
Radial increase of the cell plate area during the ring and discontinuous phragmoplast stages. Characterized by simultaneous presence of different cell plate assembly stages from cytokinetic vesicle fusion to fenestrated sheet.
Cell plate fusion site
Cortical division site
Location at which the cell plate fuses with the plasma membrane.
Cell plate initiation
Membrane trafficking and protein/protein interaction processes that lead to formation of the cell plate assembly matrix. EXOCYST and TRAPPII are both present.
Cell plate maturation
Chemical and structural modifications of the cell plate after attachment that result in cross-wall formation.
Central spindle
Central region of the anaphase spindle containing antiparallel microtubules.
[375_TD$IF]Cortical division zone (CDZ)
Zone (area) of the plasma membrane and adjacent cell wall that marks the site where the cell plate will fuse with the cell wall. CDZ is detectable during preprophase band (PPB) development and persists until completion of cell plate assembly. CDZ possesses a dynamic but distinct composition in relation to other plasma membrane and cell wall regions. The PPB is a part of the CDZ until PPB disappears during nuclear envelope breakdown.
Cross-wall
Cell plate after completing fusion with the [39_TD$IF]parental cell wall. The EXOCYST is the predominant tethering complex during cross-wall formation.
Cross-wall transformation
Chemical and structural modifications of the cross-wall that result in formation of the middle lamella.
Cytokinetic vesicles
Cell-plate-forming vesicles
Membrane vesicles that provide material for cell plate assembly. Principally of Golgi and trans-Golgi network origin and carrying both biosynthetic and endocytic material.
Discontinuous phragmoplast
Late, asymmetric
Phragmoplast after unilateral docking to the plasma membrane.
Disk phragmoplast
Solid, early, young
Phragmoplast at early cytokinetic stages, characterized by even distribution of microtubules all over the forming cell plate area.
Distal phragmoplast zone
Regions of the phragmoplast that face the daughter nuclei. The microtubule minus ends are gathered in this zone.
Division site
Region at the cortex defined by CDZ during prophase and cell plate fusion site during cytokinesis.
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Department of Plant Cell Biology, IZMB, University of Bonn, Kirschallee 1, D-53115, Bonn, Germany 4 Biology Department, University of Massachusetts, Amherst, MA 01003, USA 5 Botany Department, School of Biology and Chemistry, Osnabrück University, Barbarastraße 11, 49076 Osnabrück, Germany 6 Department of Plant Sciences, University of California Davis, Davis, CA 95616, USA 7 Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, Austria 8 Laboratory of Cell Biology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands 9 Department of Picobiology, Graduate School of Life Science, University of Hyogo, Shosha 2167, Himeji 6712201, Japan 10 Department of Plant Sciences, University of Oxford, South Parks Rd., Oxford, OX1 3RB, UK 11 Center for Plant Molecular Biology, University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany 12 National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan 13 Departments of Botany and Genetics, Laboratories of Cell and Molecular Biology, University of Wisconsin–Madison, WI, USA 14 Department of Botany, School of Biology, Aristotle University of Thessaloniki, Thessaloniki GR-541 24, Macedonia, Greece 15 Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences, University of California, Riverside, CA, USA 16 Institut de Biologie Moléculaire des Plantes, Centre National de La Recherche Scientifique, Université de Strasbourg, F67084, Strasbourgcedex, France 17 Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, Šlechtitelu 27, 783 71 Olomouc, Czech Republic 18 Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada 19 Department of [356_TD$IF]Molecular, Cellular and Developmental Biology, University of Colorado, UCB 347, Boulder, CO 80309-0347, USA 20 Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium
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Table 1. (continued) Term
Former terms
Description
Fenestrated sheet
Cell plate assembly stage characterized by expansion of the tubules within the membrane network and formation of almost continuous membrane sheet.
Fusion tubes
Membraneous cell plate extensions that connect to the parental plasma membrane during cell plate attachment.
Middle lamella
Central layer of the maturing cell plate consisting of mainly pectins, which maintains the structure and integrity of tissues by gluing adjacent cells together.
Leading zone
Outer region of the [340_TD$IF]phragmoplast.
Lagging zone
Inner region of the [341_TD$IF]expanding phragmoplast.
Peripheral microtubules
Growing microtubules at the phragmoplast leading edge that have not yet reached the midzone.
[342_TD$IF]Preprophase band (PPB)
Cortical ring of microtubules, actin filaments, cytoskeletoninteracting proteins and other components that underlies the CDZ. The PPB is connected to the nucleus by microtubules and cytoplasmic strands and to CDZ by yet unknown membrane-binding proteins. PPBs assemble during G2 [34_TD$IF]phase and disappear during prometaphase.
PPB of microtubules
Microtubule component of PPBs; a plant-specific microtubule array composed of aligned individual microtubules and bundles of mixed polarity.
Phragmoplast
Structure composed of cytoskeletal polymers, membranes, and associated cytosolic proteins that functions as the focused secretory module for assembling the cell plate.
Phragmoplast Midzone
Phragmoplast middle plane where the cell plate assembly takes place.
Phragmoplast length
Distance between the edges of opposite distal zones (Figure S3).
Ring phragmoplast
Transitional, torus, expanding, mature
Center for Plant Systems Biology, VIB, [359_TD$IF]Technologiepark 927, 9052 Ghent, Belgium 22 Department of Experimental [360_TD$IF]Plant Biology, Charles University and Institute of Experimental Botany, ASCR, Prague, Czech Republic 23 Current address: Department of Biological [361_TD$IF]Sciences, Dartmouth College, Hanover, NH 03755-3529, USA. *Correspondence: [email protected] (A. Smertenko).
Expanding phragmoplast that lacks microtubules in the center, but has not yet established contact with the plasma membrane.
Tubular network
Cell plate assembly stage characterized by interconnections between elongated membrane structures. At this stage the cell plate has smoother morphology and lower density of vesicles than the tubulovesicular network.
Tubulovesicular network
Cell plate assembly stage characterized by appearance of elongated dumbbell-shaped membrane structures.
related to polysaccharide composition of the cell plate [6] and development of plasmodesmata lie outside the scope of this work.
Cell Division Plane Determination Although our knowledge about division plane determination remains scant, we can visualize it using various markers. In a typical somatic vascular plant cell, but also in some cell types of nonvascular plants, the position of the division plane is outlined by the preprophase band (PPB). The PPB consists of a cortical ring of microtubules (Figure 1), actin filaments, organelles [e.g., endoplasmic reticulum (ER) in some species], and numerous proteins that associate with the cytoskeleton or organelles. Generally, the PPB appears as a broad array of microtubules in G2 phase and then narrows during prophase (Figures 2 and S1). Actin in the PPB is comprised of short single microfilaments, which connect adjacent microtubules and facilitate PPB narrowing (Figures 1 and 2; [7,8]). Using drugs that specifically disrupt either actin or tubulin, it appears that actin filaments require microtubules, but microtubules do not require actin to localize to the PPB [9,10].
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Table 2. Markers of Cytokinetic Structures Structure
Marker
System
[34_TD$IF]Refs
Comment
Cortical division zone (CDZ)a
Actin
Allium cepa, root apical meristem, Tradescantia virginiana, apical meristems T. virginiana, stamen hair cells
[16,17]
Excluded from CDZ
KCBP
A. thaliana root apical meristem, tobacco BY-2 cells
[53]
RanGAP
Arabidopsis thaliana, root apical meristem A. cepa, root apical meristem
[346_TD$IF][48,49]
After preprophase band (PPB) disassembly Mid- and late prophase Not apparent after PPB disassembly
POK1
A. thaliana, root apical meristem
[20]
All cell division stages
Myosin VIII
Nicotiana tabacum, tissue culture cells A. thaliana, root apical meristem Zea mays, root apical meristem Physcomitrella patens protonemal cells
[347_TD$IF][39,43]
All cell division stages All cell division stages in branching cells and from anaphase in apical cells
TAN1
A. thaliana, root apical meristem; Z. mays, leaf epidermis
[348_TD$IF][21,50]
All cell division stages
PHGAP1/2
A. thaliana, root apical meristem
[51]
Starting from anaphase
TPLATE
N. tabacum, tissue culture cells A. thaliana, root apical meristem
[42,52]
Shortly before and After cell plate attachment
KCA1
N. tabacum, tissue culture cells
[18]
Excluded from CDZ
AIR9
A. thaliana, root apical meristem
[19,53]
[349_TD$IF]Also found in PPB
POK1
A. thaliana, root apical meristem
[20]
TAN1
A. thaliana, root apical meristem; Z. mays, leaf epidermis
[348_TD$IF][21,50]
KCBP
A. thaliana, root apical meristem, tobacco BY-2 cells
[53]
PHGAP1/2
A. thaliana, root apical meristem
[51]
Myosin VIII
P. patens protonemal cells
[39]
Cell plate fusion site
Phragmoplast midzone
Phragmoplast distal zone
Cell plate
Cross-wall
a
MAP65-3
A. thaliana, root apical meristem
[32]
Myosin VIII
P. patens protonemal cells
[39]
KCBP
A. thaliana, root apical meristem
[53]
Katanin
A. thaliana, root apical meristem
[54]
AtTRS120
A. thaliana, root apical meristem
[24]
AtTRS130/CLUB
A. thaliana, root apical meristem
[24]
RAB-A1c, RAB-A1d, RAB-A1e
A. thaliana, root apical meristem
[55–57]
RAB-A2, RAB-A3
A. thaliana, root apical meristem
[23,40,56]
KNOLLE
A. thaliana, root apical meristem
[58]
KEULE
A. thaliana, root apical meristem
[25]
EXOCYST
A. thaliana, root apical meristem
[24,59]
Callose
A. thaliana, root apical meristem
[37,40,44]
All stages in branching cells and from anaphase in apical cells
Proteins that localize to CDZ after PPB disassembly.
The PPB underlies the plasma membrane region called the cortical division zone (CDZ; Figures 1 and 2). Clathrin-dependent endocytosis in this plasma membrane region is thought to mediate the localized remodeling and maintenance of the distinct molecular composition of the CDZ (Figure 2; [11]). PPB disappears at about the time of nuclear envelope breakdown in prometaphase, whereas CDZ persists throughout the ensuing stages of M phase (Table 2 [36_TD$IF]and
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Figure 1. Stages of Cytokinesis in Somatic Cells. PPB during prophase comprises aligned microtubules of mixed orientation and actin filaments. PPBs mark the CDZ. Phragmoplast initials form during the anaphase-to-telophase transition through establishment of CPAM at the region of antiparallel microtubule overlap. Short actin filaments localize along microtubules and in the CPAM. Actin filaments in the cortical cytoplasm are excluded from the CDZ. Disk phragmoplast contains the midzone occupied by the CPAM where cytokinetic vesicle fusion results in the formation of the tubulovesicular network. Many phragmoplast microtubules interact with the nuclei. Actin filaments connect the midzone to the cell cortex. Ring phragmoplast forms as the consequence of microtubules and CPAM dismantling in the central part of the phragmoplast, where cell plate assembly reaches tubular network stage. New antiparallel microtubule overlaps in the phragmoplast midzone facilitate CPAM formation and cell plate assembly. Actin filaments connect the phragmoplast leading zone with the CDZ and guide phragmoplast expansion. The phragmoplast expands gradually until it reaches the plasma membrane. Discontinuous phragmoplast forms when microtubules are lost at the sites of cell plate attachment to the plasma membrane. Peripheral microtubules come in contact with the cell cortex and then cell plate extensions fusion tubes connect to the cell plate fusion site at the plasma membrane. Cross-wall is the product of cell plate maturation. Primary cell wall synthesis and chemical transformation of cross-wall continues during interphase. Abbreviations: CDZ, cortical division zone; CPAM, cell plate assembly matrix; PPB, preprophase band.
Figure S2). Whether the PPB actively defines the division plane or just responds to yet unknown cues remains an open question. Recent work shows that in some cell types the PPB of microtubules is dispensable for the determination of the division plane [12], but increases the precision of spindle alignment with the division plane [12,13]. Nuclear location appears to play
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Figure 2. B [35_TD$IF] iogenesis of the PPB of Microtubules. The PPB of microtubules appears as an aligned array in the cortical cytoplasm in late G2 phase (1, 2). During prophase, the PPB narrows down and actin filaments concentrate in the PPB region (3). Protein linkers can attach microtubules to the plasma membrane or actin filaments; clathrin-dependent endocytosis alters the molecular composition of the plasma membrane and the scaffold in the PPB region (zoom of the boxed region). Towards the end of prophase microtubules form a tight band, which lacks actin filaments; actin filaments are present in other parts of the cell cortex (4). Microtubules disappear during prometaphase, leaving behind unique composition of the scaffold and membrane proteins (5). Abbreviations: PPB, preprophase band; CDZ, cortical division zone.
an active role in positioning the PPB as displacement of the nucleus by centrifugation causes formation of two PPBs: at the former and new site of the nucleus [14,15]. The CDZ maintains a distinct but dynamic protein composition throughout the remaining stages of cell division. For example, the TPLATE protein associates with the CDZ at the end of cytokinesis, when the cell plate attaches to the plasma membrane and the parental cell wall. TPLATE, a part of an early adaptor complex involved in endocytosis, is proposed to function to confine cell plate proteins, such as the SNARE protein KNOLLE, to the cell plate. Although actin filaments localize to the PPB and, in the same manner as microtubules, form a band that narrows during PPB development, actin filaments become excluded from the CDZ in many cell types in late prophase to form an actin-depleted zone (ADZ) [16,17]. In some types of cells, actin filaments are enriched at either side of the ADZ and called twin peaks. Additionally, other proteins (e.g., kinesin KCA1; [18]) are excluded from the CDZ. At the end of prophase the nuclear envelope breaks down and this is followed by the formation of an acentriolar spindle. The chromosomes in the metaphase spindle are usually aligned at the division plane. During anaphase, the central spindle forms roughly at the site of the metaphase chromosomes. Thus, the position of both metaphase and anaphase spindles apparently responds to cues that maintain the division plane. The nature of these cues remains unknown, but they are likely produced in the CDZ. As a cell progresses towards telophase, some division site markers become confined to the future cell plate fusion site (Table 2). Typically, the cell plate fusion site bisects the CDZ. Distinct molecular composition (e.g., TPLATE) suggests that the cell plate fusion site and CDZ represent distinct plasma-membrane domains. In cells treated with [364_TD$IF]herbicide chlorpropham, or in various mutants, including tangled1, phragmoplast orienting kinesin1 (pok1), and pok2, the cell plate attaches at a site that lies outside the CDZ, indicating that cell plate fusion can occur without CDZ components [19–21].
Cell Plate Assembly Cell plate assembly occurs by the cooperation of the post-Golgi endomembrane system and the phragmoplast, which consists of a bipolar array of microtubules and actin filaments
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(Figures 1 and S3). The phragmoplast originates from antiparallel microtubules of the central spindle (phragmoplast initials in Figure 1) and at early stages looks like a disk in light micrographs (Figure S3A,[365_TD$IF]B). The majority of microtubule plus ends face the central plane of the phragmoplast or phragmoplast midzone, while minus ends are pointed towards the distal zones (Figure S3B). Cell plate assembly starts during the anaphase-to-telophase transition with the formation of an entity called the cell plate assembly matrix (CPAM) at the phragmoplast midzone (Figure 1; [22]). The processes underlying CPAM formation are collectively named cell plate initiation. In electron micrographs of cryofixed cells, CPAM appears as a ribosome-free zone flanking the cell plate (meaning that it might have pores with size <20 nm) within which the cytokinetic vesicles interact and fuse. The structural proteins of the CPAM have not been identified yet, but electron microscopy, live-cell imaging, and immunofluorescence microscopy show that the phragmoplast midzone contains Golgi- and trans-Golgi network (TGN)-derived vesicles and vesicle-associated molecular machinery, including small Rab GTPases, such as the Rab-A2 subclass, RAB-A3, and RAB-A1d; SNARE proteins, such as the syntaxin KNOLLE; transport protein particle (TRAPP)II; dynamin-related proteins; EXOCYST tethering complexes; and actin. Mutant analysis has pointed to different roles for some of these molecules in cell plate assembly [23–26]. The delivery to, tethering at, and subsequent fusion of cytokinetic vesicles within [36_TD$IF]the CPAM results in cell plate biogenesis and expansion. Positioning of the CPAM appears to be related to the fact that the CPAM molecules are delivered from both sides of the phragmoplast and, owing presumably to their affinity, assemble where they meet. However, the signal for exactly where the assembly occurs has yet to be identified. One hypothesis, based on research in Physcomitrella patens, is that CPAM location is determined by overlap of microtubules with opposite polarity (antiparallel microtubules; [27]). Overlapping microtubule plus ends that originate from opposite distal zones become bundled and stabilized by crosslinking protein microtubule-associated protein (MAP)65 and kinesin-4. Initial membrane depositions in the phragmoplast midzone colocalize with MAP65 proteins, which have been shown to interact genetically and/or physically with phospholipids and with the TRAPPII-tethering complex [26–28]. Although MAP65-dependent spatial organization of microtubules in the phragmoplast midzone has been supported by genetics [29–32], electron microscopy [30,33], immunofluorescence [30,34], and live-cell imaging [29,35], using electron tomography no microtubule overlap was observed in the phragmoplast midzone of Arabidopsis root apical meristem cells [36]. Thus, more research is necessary to understand the role of antiparallel microtubule bundling and MAP65 proteins in the phragmoplast organization, CPAM formation, and subsequent stages of cell plate assembly. Transmission electron microscopy and tomography data reveal four stages of cell plate assembly: (i) accumulation and fusion of vesicles; (ii) tubulovesicular network; (iii) tubular network; and (iv) fenestrated sheet [37]. The first two stages take place inside the CPAM. Visualization of microtubules in the phragmoplast with established CPAM using live-cell imaging or immunofluorescence microscopy reveals the phragmoplast midzone as a dark line (Figure S3A). Consistent with the light microscopy images, electron tomography reconstructions demonstrate that only 0.8% of phragmoplast microtubules terminate in the cell plate proximity, while 65% of microtubules terminate inside and 34% outside the CPAM [36], suggesting that the CPAM can capture and stabilize the plus ends of phragmoplast microtubules independently of the antiparallel microtubule overlap regions. The diameter of the disk phragmoplast approximately equals that of the daughter nuclei. However, cells are generally wider than the nuclei and, in order to complete cell plate synthesis,
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the phragmoplast expands (translocates) centrifugally towards the CDZ and appears as a ring (Figures 1 and S3). Expansion proceeds as microtubules are disassembled in the inner region (lagging zone), and new microtubules polymerize at the outer phragmoplast edge (leading zone). Tubulin released in the lagging zone is recycled for the polymerization of new microtubules in the leading zone. Overlapping antiparallel microtubules crosslinked by MAP65 are continuously formed in the leading zone [38]. These overlap regions structurally stabilize the midzone and initiate CPAM formation where the next round of cell plate assembly takes place. Actin filaments are largely polymerized at the leading edge, extending out towards the cell cortex and actively attaching at the CDZ. Myosins on the plus ends of microtubules can interact with the actin meshwork thereby guiding phragmoplast expansion to the division site (as exemplified by myosin VIII in P. patens; [39]). Within the central region of the microtubule ring, formed by the breakdown of microtubules in the central region of the disk phragmoplast and assembly of new microtubules at the leading zone, the growing cell plate becomes a calloserich interconnected tubular network. Remodeling of membrane and cell plate material through clathrin-mediated endocytosis leads to the formation of the planar fenestrated sheet. All stages of cell plate assembly coexist in the expanding phragmoplast. Consequently, the spatiotemporal distribution of individual membrane proteins that contribute to different cell plate assembly processes in the phragmoplast can be different ([25,40]; compare RAB-A2a and KNOLLE in Figure S2). As the phragmoplast often forms off cell center, the attachment of the cell plate to the cell plate fusion site first occurs at one site and then progresses to other sites until the fusion is complete (Figures 1 and S3; [41]). Prior to cell plate attachment, peripheral phragmoplast microtubules at the leading zone interact with the cortex. Then finger-shaped membrane structures (fusion tubes) attach the cell plate to the cell plate fusion site [22,37]. This attachment could be important for stabilizing the position of the cell plate; however, it remains unknown whether attachment site selection within CDZ is stochastic or results from a polarized translocation of the phragmoplast towards a specific position at cell plate fusion site. Microtubules depolymerize at the attachment site, resulting in a discontinuous phragmoplast (Figures 1 and S3). What signals guide the centrifugal expansion remains unknown, but actin filaments have been shown to play a key role in guiding phragmoplast expansion and final positioning of the cell plate. Depolymerization of microtubules following cell plate fusion events results in fragments of phragmoplast scattered along the perimeter of the cell plate fusion site (Figure S3). Upon cell plate fusion, the lumen of the cell plate is continuous with the apoplast and its physicochemical properties subsequently mature into primary cell wall. In addition, the attachment allows diffusion of plasma-membrane proteins and lipids from plasma membrane to the cell plate. These changes trigger a novel phase in cell plate assembly, which has been referred to as cell plate maturation. After attachment, the TRAPPII complex disappears from the cell plate and EXOCYST becomes the predominant tethering complex [24]. This marks a change in trafficking to the cell plate. For example, TPLATE and myosin VIII have been shown to be specifically recruited to the cell plate only after attachment [42,43]. Cell plate maturation results in a cross-wall, which in addition to callose [37,40,44], contains cellulose, hemicellulose, and pectin [45–47]. The cross-wall gradually develops a pectin-rich middle lamella as the cellulose– hemicellulose networks are assembled on the opposite cell plate membranes. However the distinct stages of polysaccharide deposition during cell plate maturation and cross-wall transformation remain to be characterized [6]. Integration of the cross-wall with the [39_TD$IF]parental cell wall involves localized digestion of the cellulose layer of the [39_TD$IF]parental cell wall at the attachment site to enable the middle lamellae of the two walls to form a continuum. The formation of the cross-wall hallmarks completion of the cytokinesis and establishment of the two daughter cells.
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Concluding Remarks
Outstanding Questions
Exciting research of the [367_TD$IF]past decade has not only significantly boosted understanding of plant cytokinesis, but also demonstrated a high degree of complexity of the self-organization processes responsible for both cell plate positioning and formation. The revised terminology aims to capture this complexity and highlights emerging concepts in the plant cytokinesis field. [368_TD$IF]Our work will facilitate addressing the extensive gaps in our knowledge of plant cell cytokinesis (see Outstanding Questions).
How are PPB, ADZ, and cortical division zones spatially and temporarily regulated? How are actin filaments depleted from the ADZ? What changes in membrane proteins and lipids accompany CDZ formation? Do these changes involve interactions with the cell wall?
Acknowledgments Images of dividing BY-2 cells in Figure S3A were taken by Laining Zhang and Deirdre Fahy; images of TAN1 and tubulin were provided by Pablo Martinez. We thank Alex Steiner for support with the assembly of [37_TD$IF]Figure S2 panels. This work was supported by USDA-NIFA hatch grant WNP00826 and WSU startup fund (to AS). EP is supported by the AUTh Research Committee (grant No. [370_TD$IF]91913) by funds of Schur Flexibles Group. CR is supported by NSF-MCB#1505848. IM is supported by BBSRC BB/I022996/1. JŠ is supported by grant No. LO1204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I, MEYS. The authors are grateful to Tobias Baskin, Tijs Ketelaar, and Gohta Goshima for their critical comments on the manuscript. We are also thankful to Bo Liu for encouraging this project.
What factors define microtubule and actin filament organization and trigger their reorganization during phragmoplast expansion? How and to what extent do microtubules and actin filaments need to cooperate to enable correct guidance of the phragmoplast? How does cytokinesis differ between cells that form and do not form a PPB? How do actin filaments guide the phragmoplast expansion?
Supplemental Information Supplemental information associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. tcb.2017.08.008.
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CPAM: what proteins constitute CPAM and how are they interconnected? Do the scaffold-forming proteins possess different binding sites for different proteins that localize to the CPAM? How is their assembly and disassembly regulated? How does the CPAM exclude ribosomes while allowing the larger cytokinetic vesicles to reach the forming cell plate? What is the function of actin in the CPAM? Cell plate assembly: how do the proteins in the antiparallel microtubule overlap region contribute to cell plate assembly? How are cytokinetic vesicles delivered to the phragmoplast midzone? How are the transitions between the cell plate assembly stages coordinated with microtubule dynamics and phragmoplast organization? Do vesicles involved in cell plate assembly have different molecular composition and cargo? Positioning of nucleus, ER, Golgi and TGN: how does the position of the nucleus during G2 affect the location of the cell division plane? What factors control the reorganization of the ER and the positioning of Golgi and TGN during cytokinesis? Is the repositioning of the Golgi and TGN prior to cytokinesis linked to changes in content of the cytokinetic vesicles? What are the stages of polysaccharide deposition during the transformation of the cell plate to a new cell wall and middle lamella?
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44. Thiele, K. et al. (2009) The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant J. 58, 13–26 45. Baluska, F. et al. (2005) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225, 141–155 46. Fujita, M. and Wasteneys, G.O. (2014) A survey of cellulose microfibril patterns in dividing, expanding, and differentiating cells of Arabidopsis thaliana. Protoplasma 251, 687–698 47. Miart, F. et al. (2014) Spatio-temporal analysis of cellulose synthesis during cell plate formation in Arabidopsis. Plant J. 77, 71–84 48. Xu, X.M. et al. (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc. Natl. Acad. Sci. U. S. A. 105, 18637–18642 49. Yabuuchi, T. et al. (2015) Preprophase band formation and cortical division zone establishment: RanGAP behaves differently from microtubules during their band formation. Plant Signal. Behav. 10, e1060385 50. Walker, K.L. et al. (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr. Biol. 17, 1827–1836 51. Stöckle, D. et al. (2016) Putative RopGAPs impact division plane selection and interact with kinesin-12 POK1. Nat. Plants 2, 16120 52. van Damme, D. et al. (2006) Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 18, 3502–3518 53. Buschmann, H. et al. (2015) Arabidopsis KCBP interacts with AIR9 but stays in the cortical division zone throughout mitosis via its MyTH4–FERM domain. J. Cell Sci. 128, 2033–2046
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59. Fendrych, M. et al. (2010) The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell 22, 3053–3065
Opinion
Plant Cytokinesis: Terminology for Structures and Processes Andrei Smertenko,1,* Farhah Assaad,2 František Baluška,3 Magdalena Bezanilla,4,23 Henrik Buschmann,5 Georgia Drakakaki,6 Marie-Theres Hauser,7 Marcel Janson,8 Yoshinobu Mineyuki,9 Ian Moore,10 Sabine Müller,11 Takashi Murata,12 Marisa S. Otegui,13 Emmanuel Panteris,14 Carolyn Rasmussen,15 Anne-Catherine Schmit,16 Jozef Šamaj,17 Lacey Samuels,18 L. Andrew Staehelin,19 Daniel Van Damme,20,21 Geoffrey Wasteneys,18 and Viktor Žárský22 Plant cytokinesis is orchestrated by a specialized structure, the phragmoplast. The phragmoplast first occurred in representatives of Charophyte algae and then became the main division apparatus in land plants. Major cellular activities, including cytoskeletal dynamics, vesicle trafficking, membrane assembly, and cell wall biosynthesis, cooperate in the phragmoplast under the guidance of a complex signaling network. Furthermore, the phragmoplast combines plant-specific features with the conserved cytokinetic processes of animals, fungi, and protists. As such, the phragmoplast represents a useful system for understanding both plant cell dynamics and the evolution of cytokinesis. We recognize that future research and knowledge transfer into other fields would benefit from standardized terminology. Here, we propose such a lexicon of terminology for specific structures and processes associated with plant cytokinesis.
Trends A large number of phragmoplast proteins have been identified. Electron microscopy/tomography studies have produced nanoscale information about the architecture of phragmoplast and cell plate assembly stages in cryofixed cells. Novel components of the cortical division zone and cell plate fusion site have been discovered. This information lays a foundation for understanding how plant cells memorize the division plane throughout mitosis and how the cell plate is guided to its predetermined attachment site.
Rationale for Updating Plant Cytokinesis Terminology Current plant cytokinesis terminology was developed using data generated by fluorescence microscopy of live or fixed cells, electron microscopy of chemically or cryofixed cells, and genetic strategies. As a consequence of different experimental approaches, and for historic reasons, the cytokinetic processes and structures are often referred to by different names. Because plant cytokinesis has become a useful model system for addressing specific questions in plant biochemistry, cell biology, development, etc., we recognize that exchange of information between scientists working in these diverse fields, as well as further advancement of plant cytokinesis research, would benefit from a harmonized terminology. Here, we summarize the steps[376_TD$IF], and update terminology associated with two major processes in plant cytokinesis: determination of the cell division plane and assembly of the cell plate (Table 1). We also propose established markers for some processes and structures (Table 2). The terminology proposed here uses cytokinesis in somatic cells as an example and takes advantage of available structural information. Division in reproductive organs and specialized cell types involves similar processes, which appear to be structurally different [1]. For in-depth description of cytokinesis in somatic cells we refer to several recent reviews [2–6]. Terminology
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MAP65 and plus end-directed kinesins contribute to the maintenance of the antiparallel overlap of phragmoplast microtubules. In addition, the MAP65–TRAPPII interaction plays a key role in cell plate assembly. Actin filaments align parallel to microtubules in the phragmoplast, while some microfilaments extend from cell plate margin to guide its expansion towards the fusion site.
1
Institute of Biological Chemistry, Washington State University, Pullman, WA 99164, USA 2 Botany Department, WZW, Technische Universität München, Freising, 85354 Germany
http://dx.doi.org/10.1016/j.tcb.2017.08.008 © 2017 Elsevier Ltd. All rights reserved.
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Table 1. Glossary of [374_TD$IF]Plant Cytokinesis Terminology Term
Former terms
Description Cortical region of cytoplasm with few actin filaments that forms prior to nuclear envelope breakdown and usually coincides with the cortical division zone (CDZ). ADZ can be flanked by domains enriched in actin filaments, known as a twin-peaks structure in some cell types.
Actin-depleted zone (ADZ)
Cell division plane
Anticipated or true position of the cell plate.
Cell plate
Membrane-polysaccharide compartment that partitions the cytoplasm after nuclear division.
Cell plate assembly
General term referring to all processes from cell plate biogenesis to maturation.
Cell plate assembly matrix (CPAM)
Amorphous scaffold system consisting of proteins and vesicles in the phragmoplast midzone (150 nm thick) that is responsible for mobilization of protein complexes and vesicles involved in cell plate assembly.
Cell plate attachment
Process of cell plate anchoring and fusion to the parental plasma membrane and cell wall.
Cell plate biogenesis
Generation of a membrane compartment via vesicle tethering and fusion inside the CPAM. Transport protein particle (TRAPP)II is the predominant tethering complex.
Cell plate expansion
Radial increase of the cell plate area during the ring and discontinuous phragmoplast stages. Characterized by simultaneous presence of different cell plate assembly stages from cytokinetic vesicle fusion to fenestrated sheet.
Cell plate fusion site
Cortical division site
Location at which the cell plate fuses with the plasma membrane.
Cell plate initiation
Membrane trafficking and protein/protein interaction processes that lead to formation of the cell plate assembly matrix. EXOCYST and TRAPPII are both present.
Cell plate maturation
Chemical and structural modifications of the cell plate after attachment that result in cross-wall formation.
Central spindle
Central region of the anaphase spindle containing antiparallel microtubules.
[375_TD$IF]Cortical division zone (CDZ)
Zone (area) of the plasma membrane and adjacent cell wall that marks the site where the cell plate will fuse with the cell wall. CDZ is detectable during preprophase band (PPB) development and persists until completion of cell plate assembly. CDZ possesses a dynamic but distinct composition in relation to other plasma membrane and cell wall regions. The PPB is a part of the CDZ until PPB disappears during nuclear envelope breakdown.
Cross-wall
Cell plate after completing fusion with the [39_TD$IF]parental cell wall. The EXOCYST is the predominant tethering complex during cross-wall formation.
Cross-wall transformation
Chemical and structural modifications of the cross-wall that result in formation of the middle lamella.
Cytokinetic vesicles
Cell-plate-forming vesicles
Membrane vesicles that provide material for cell plate assembly. Principally of Golgi and trans-Golgi network origin and carrying both biosynthetic and endocytic material.
Discontinuous phragmoplast
Late, asymmetric
Phragmoplast after unilateral docking to the plasma membrane.
Disk phragmoplast
Solid, early, young
Phragmoplast at early cytokinetic stages, characterized by even distribution of microtubules all over the forming cell plate area.
Distal phragmoplast zone
Regions of the phragmoplast that face the daughter nuclei. The microtubule minus ends are gathered in this zone.
Division site
Region at the cortex defined by CDZ during prophase and cell plate fusion site during cytokinesis.
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Department of Plant Cell Biology, IZMB, University of Bonn, Kirschallee 1, D-53115, Bonn, Germany 4 Biology Department, University of Massachusetts, Amherst, MA 01003, USA 5 Botany Department, School of Biology and Chemistry, Osnabrück University, Barbarastraße 11, 49076 Osnabrück, Germany 6 Department of Plant Sciences, University of California Davis, Davis, CA 95616, USA 7 Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, Austria 8 Laboratory of Cell Biology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands 9 Department of Picobiology, Graduate School of Life Science, University of Hyogo, Shosha 2167, Himeji 6712201, Japan 10 Department of Plant Sciences, University of Oxford, South Parks Rd., Oxford, OX1 3RB, UK 11 Center for Plant Molecular Biology, University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany 12 National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan 13 Departments of Botany and Genetics, Laboratories of Cell and Molecular Biology, University of Wisconsin–Madison, WI, USA 14 Department of Botany, School of Biology, Aristotle University of Thessaloniki, Thessaloniki GR-541 24, Macedonia, Greece 15 Center for Plant Cell Biology, Institute of Integrative Genome Biology, Department of Botany and Plant Sciences, University of California, Riverside, CA, USA 16 Institut de Biologie Moléculaire des Plantes, Centre National de La Recherche Scientifique, Université de Strasbourg, F67084, Strasbourgcedex, France 17 Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, Šlechtitelu 27, 783 71 Olomouc, Czech Republic 18 Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada 19 Department of [356_TD$IF]Molecular, Cellular and Developmental Biology, University of Colorado, UCB 347, Boulder, CO 80309-0347, USA 20 Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium
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Table 1. (continued) Term
Former terms
Description
Fenestrated sheet
Cell plate assembly stage characterized by expansion of the tubules within the membrane network and formation of almost continuous membrane sheet.
Fusion tubes
Membraneous cell plate extensions that connect to the parental plasma membrane during cell plate attachment.
Middle lamella
Central layer of the maturing cell plate consisting of mainly pectins, which maintains the structure and integrity of tissues by gluing adjacent cells together.
Leading zone
Outer region of the [340_TD$IF]phragmoplast.
Lagging zone
Inner region of the [341_TD$IF]expanding phragmoplast.
Peripheral microtubules
Growing microtubules at the phragmoplast leading edge that have not yet reached the midzone.
[342_TD$IF]Preprophase band (PPB)
Cortical ring of microtubules, actin filaments, cytoskeletoninteracting proteins and other components that underlies the CDZ. The PPB is connected to the nucleus by microtubules and cytoplasmic strands and to CDZ by yet unknown membrane-binding proteins. PPBs assemble during G2 [34_TD$IF]phase and disappear during prometaphase.
PPB of microtubules
Microtubule component of PPBs; a plant-specific microtubule array composed of aligned individual microtubules and bundles of mixed polarity.
Phragmoplast
Structure composed of cytoskeletal polymers, membranes, and associated cytosolic proteins that functions as the focused secretory module for assembling the cell plate.
Phragmoplast Midzone
Phragmoplast middle plane where the cell plate assembly takes place.
Phragmoplast length
Distance between the edges of opposite distal zones (Figure S3).
Ring phragmoplast
Transitional, torus, expanding, mature
Center for Plant Systems Biology, VIB, [359_TD$IF]Technologiepark 927, 9052 Ghent, Belgium 22 Department of Experimental [360_TD$IF]Plant Biology, Charles University and Institute of Experimental Botany, ASCR, Prague, Czech Republic 23 Current address: Department of Biological [361_TD$IF]Sciences, Dartmouth College, Hanover, NH 03755-3529, USA. *Correspondence: [email protected] (A. Smertenko).
Expanding phragmoplast that lacks microtubules in the center, but has not yet established contact with the plasma membrane.
Tubular network
Cell plate assembly stage characterized by interconnections between elongated membrane structures. At this stage the cell plate has smoother morphology and lower density of vesicles than the tubulovesicular network.
Tubulovesicular network
Cell plate assembly stage characterized by appearance of elongated dumbbell-shaped membrane structures.
related to polysaccharide composition of the cell plate [6] and development of plasmodesmata lie outside the scope of this work.
Cell Division Plane Determination Although our knowledge about division plane determination remains scant, we can visualize it using various markers. In a typical somatic vascular plant cell, but also in some cell types of nonvascular plants, the position of the division plane is outlined by the preprophase band (PPB). The PPB consists of a cortical ring of microtubules (Figure 1), actin filaments, organelles [e.g., endoplasmic reticulum (ER) in some species], and numerous proteins that associate with the cytoskeleton or organelles. Generally, the PPB appears as a broad array of microtubules in G2 phase and then narrows during prophase (Figures 2 and S1). Actin in the PPB is comprised of short single microfilaments, which connect adjacent microtubules and facilitate PPB narrowing (Figures 1 and 2; [7,8]). Using drugs that specifically disrupt either actin or tubulin, it appears that actin filaments require microtubules, but microtubules do not require actin to localize to the PPB [9,10].
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Table 2. Markers of Cytokinetic Structures Structure
Marker
System
[34_TD$IF]Refs
Comment
Cortical division zone (CDZ)a
Actin
Allium cepa, root apical meristem, Tradescantia virginiana, apical meristems T. virginiana, stamen hair cells
[16,17]
Excluded from CDZ
KCBP
A. thaliana root apical meristem, tobacco BY-2 cells
[53]
RanGAP
Arabidopsis thaliana, root apical meristem A. cepa, root apical meristem
[346_TD$IF][48,49]
After preprophase band (PPB) disassembly Mid- and late prophase Not apparent after PPB disassembly
POK1
A. thaliana, root apical meristem
[20]
All cell division stages
Myosin VIII
Nicotiana tabacum, tissue culture cells A. thaliana, root apical meristem Zea mays, root apical meristem Physcomitrella patens protonemal cells
[347_TD$IF][39,43]
All cell division stages All cell division stages in branching cells and from anaphase in apical cells
TAN1
A. thaliana, root apical meristem; Z. mays, leaf epidermis
[348_TD$IF][21,50]
All cell division stages
PHGAP1/2
A. thaliana, root apical meristem
[51]
Starting from anaphase
TPLATE
N. tabacum, tissue culture cells A. thaliana, root apical meristem
[42,52]
Shortly before and After cell plate attachment
KCA1
N. tabacum, tissue culture cells
[18]
Excluded from CDZ
AIR9
A. thaliana, root apical meristem
[19,53]
[349_TD$IF]Also found in PPB
POK1
A. thaliana, root apical meristem
[20]
TAN1
A. thaliana, root apical meristem; Z. mays, leaf epidermis
[348_TD$IF][21,50]
KCBP
A. thaliana, root apical meristem, tobacco BY-2 cells
[53]
PHGAP1/2
A. thaliana, root apical meristem
[51]
Myosin VIII
P. patens protonemal cells
[39]
Cell plate fusion site
Phragmoplast midzone
Phragmoplast distal zone
Cell plate
Cross-wall
a
MAP65-3
A. thaliana, root apical meristem
[32]
Myosin VIII
P. patens protonemal cells
[39]
KCBP
A. thaliana, root apical meristem
[53]
Katanin
A. thaliana, root apical meristem
[54]
AtTRS120
A. thaliana, root apical meristem
[24]
AtTRS130/CLUB
A. thaliana, root apical meristem
[24]
RAB-A1c, RAB-A1d, RAB-A1e
A. thaliana, root apical meristem
[55–57]
RAB-A2, RAB-A3
A. thaliana, root apical meristem
[23,40,56]
KNOLLE
A. thaliana, root apical meristem
[58]
KEULE
A. thaliana, root apical meristem
[25]
EXOCYST
A. thaliana, root apical meristem
[24,59]
Callose
A. thaliana, root apical meristem
[37,40,44]
All stages in branching cells and from anaphase in apical cells
Proteins that localize to CDZ after PPB disassembly.
The PPB underlies the plasma membrane region called the cortical division zone (CDZ; Figures 1 and 2). Clathrin-dependent endocytosis in this plasma membrane region is thought to mediate the localized remodeling and maintenance of the distinct molecular composition of the CDZ (Figure 2; [11]). PPB disappears at about the time of nuclear envelope breakdown in prometaphase, whereas CDZ persists throughout the ensuing stages of M phase (Table 2 [36_TD$IF]and
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Figure 1. Stages of Cytokinesis in Somatic Cells. PPB during prophase comprises aligned microtubules of mixed orientation and actin filaments. PPBs mark the CDZ. Phragmoplast initials form during the anaphase-to-telophase transition through establishment of CPAM at the region of antiparallel microtubule overlap. Short actin filaments localize along microtubules and in the CPAM. Actin filaments in the cortical cytoplasm are excluded from the CDZ. Disk phragmoplast contains the midzone occupied by the CPAM where cytokinetic vesicle fusion results in the formation of the tubulovesicular network. Many phragmoplast microtubules interact with the nuclei. Actin filaments connect the midzone to the cell cortex. Ring phragmoplast forms as the consequence of microtubules and CPAM dismantling in the central part of the phragmoplast, where cell plate assembly reaches tubular network stage. New antiparallel microtubule overlaps in the phragmoplast midzone facilitate CPAM formation and cell plate assembly. Actin filaments connect the phragmoplast leading zone with the CDZ and guide phragmoplast expansion. The phragmoplast expands gradually until it reaches the plasma membrane. Discontinuous phragmoplast forms when microtubules are lost at the sites of cell plate attachment to the plasma membrane. Peripheral microtubules come in contact with the cell cortex and then cell plate extensions fusion tubes connect to the cell plate fusion site at the plasma membrane. Cross-wall is the product of cell plate maturation. Primary cell wall synthesis and chemical transformation of cross-wall continues during interphase. Abbreviations: CDZ, cortical division zone; CPAM, cell plate assembly matrix; PPB, preprophase band.
Figure S2). Whether the PPB actively defines the division plane or just responds to yet unknown cues remains an open question. Recent work shows that in some cell types the PPB of microtubules is dispensable for the determination of the division plane [12], but increases the precision of spindle alignment with the division plane [12,13]. Nuclear location appears to play
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Figure 2. B [35_TD$IF] iogenesis of the PPB of Microtubules. The PPB of microtubules appears as an aligned array in the cortical cytoplasm in late G2 phase (1, 2). During prophase, the PPB narrows down and actin filaments concentrate in the PPB region (3). Protein linkers can attach microtubules to the plasma membrane or actin filaments; clathrin-dependent endocytosis alters the molecular composition of the plasma membrane and the scaffold in the PPB region (zoom of the boxed region). Towards the end of prophase microtubules form a tight band, which lacks actin filaments; actin filaments are present in other parts of the cell cortex (4). Microtubules disappear during prometaphase, leaving behind unique composition of the scaffold and membrane proteins (5). Abbreviations: PPB, preprophase band; CDZ, cortical division zone.
an active role in positioning the PPB as displacement of the nucleus by centrifugation causes formation of two PPBs: at the former and new site of the nucleus [14,15]. The CDZ maintains a distinct but dynamic protein composition throughout the remaining stages of cell division. For example, the TPLATE protein associates with the CDZ at the end of cytokinesis, when the cell plate attaches to the plasma membrane and the parental cell wall. TPLATE, a part of an early adaptor complex involved in endocytosis, is proposed to function to confine cell plate proteins, such as the SNARE protein KNOLLE, to the cell plate. Although actin filaments localize to the PPB and, in the same manner as microtubules, form a band that narrows during PPB development, actin filaments become excluded from the CDZ in many cell types in late prophase to form an actin-depleted zone (ADZ) [16,17]. In some types of cells, actin filaments are enriched at either side of the ADZ and called twin peaks. Additionally, other proteins (e.g., kinesin KCA1; [18]) are excluded from the CDZ. At the end of prophase the nuclear envelope breaks down and this is followed by the formation of an acentriolar spindle. The chromosomes in the metaphase spindle are usually aligned at the division plane. During anaphase, the central spindle forms roughly at the site of the metaphase chromosomes. Thus, the position of both metaphase and anaphase spindles apparently responds to cues that maintain the division plane. The nature of these cues remains unknown, but they are likely produced in the CDZ. As a cell progresses towards telophase, some division site markers become confined to the future cell plate fusion site (Table 2). Typically, the cell plate fusion site bisects the CDZ. Distinct molecular composition (e.g., TPLATE) suggests that the cell plate fusion site and CDZ represent distinct plasma-membrane domains. In cells treated with [364_TD$IF]herbicide chlorpropham, or in various mutants, including tangled1, phragmoplast orienting kinesin1 (pok1), and pok2, the cell plate attaches at a site that lies outside the CDZ, indicating that cell plate fusion can occur without CDZ components [19–21].
Cell Plate Assembly Cell plate assembly occurs by the cooperation of the post-Golgi endomembrane system and the phragmoplast, which consists of a bipolar array of microtubules and actin filaments
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(Figures 1 and S3). The phragmoplast originates from antiparallel microtubules of the central spindle (phragmoplast initials in Figure 1) and at early stages looks like a disk in light micrographs (Figure S3A,[365_TD$IF]B). The majority of microtubule plus ends face the central plane of the phragmoplast or phragmoplast midzone, while minus ends are pointed towards the distal zones (Figure S3B). Cell plate assembly starts during the anaphase-to-telophase transition with the formation of an entity called the cell plate assembly matrix (CPAM) at the phragmoplast midzone (Figure 1; [22]). The processes underlying CPAM formation are collectively named cell plate initiation. In electron micrographs of cryofixed cells, CPAM appears as a ribosome-free zone flanking the cell plate (meaning that it might have pores with size <20 nm) within which the cytokinetic vesicles interact and fuse. The structural proteins of the CPAM have not been identified yet, but electron microscopy, live-cell imaging, and immunofluorescence microscopy show that the phragmoplast midzone contains Golgi- and trans-Golgi network (TGN)-derived vesicles and vesicle-associated molecular machinery, including small Rab GTPases, such as the Rab-A2 subclass, RAB-A3, and RAB-A1d; SNARE proteins, such as the syntaxin KNOLLE; transport protein particle (TRAPP)II; dynamin-related proteins; EXOCYST tethering complexes; and actin. Mutant analysis has pointed to different roles for some of these molecules in cell plate assembly [23–26]. The delivery to, tethering at, and subsequent fusion of cytokinetic vesicles within [36_TD$IF]the CPAM results in cell plate biogenesis and expansion. Positioning of the CPAM appears to be related to the fact that the CPAM molecules are delivered from both sides of the phragmoplast and, owing presumably to their affinity, assemble where they meet. However, the signal for exactly where the assembly occurs has yet to be identified. One hypothesis, based on research in Physcomitrella patens, is that CPAM location is determined by overlap of microtubules with opposite polarity (antiparallel microtubules; [27]). Overlapping microtubule plus ends that originate from opposite distal zones become bundled and stabilized by crosslinking protein microtubule-associated protein (MAP)65 and kinesin-4. Initial membrane depositions in the phragmoplast midzone colocalize with MAP65 proteins, which have been shown to interact genetically and/or physically with phospholipids and with the TRAPPII-tethering complex [26–28]. Although MAP65-dependent spatial organization of microtubules in the phragmoplast midzone has been supported by genetics [29–32], electron microscopy [30,33], immunofluorescence [30,34], and live-cell imaging [29,35], using electron tomography no microtubule overlap was observed in the phragmoplast midzone of Arabidopsis root apical meristem cells [36]. Thus, more research is necessary to understand the role of antiparallel microtubule bundling and MAP65 proteins in the phragmoplast organization, CPAM formation, and subsequent stages of cell plate assembly. Transmission electron microscopy and tomography data reveal four stages of cell plate assembly: (i) accumulation and fusion of vesicles; (ii) tubulovesicular network; (iii) tubular network; and (iv) fenestrated sheet [37]. The first two stages take place inside the CPAM. Visualization of microtubules in the phragmoplast with established CPAM using live-cell imaging or immunofluorescence microscopy reveals the phragmoplast midzone as a dark line (Figure S3A). Consistent with the light microscopy images, electron tomography reconstructions demonstrate that only 0.8% of phragmoplast microtubules terminate in the cell plate proximity, while 65% of microtubules terminate inside and 34% outside the CPAM [36], suggesting that the CPAM can capture and stabilize the plus ends of phragmoplast microtubules independently of the antiparallel microtubule overlap regions. The diameter of the disk phragmoplast approximately equals that of the daughter nuclei. However, cells are generally wider than the nuclei and, in order to complete cell plate synthesis,
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the phragmoplast expands (translocates) centrifugally towards the CDZ and appears as a ring (Figures 1 and S3). Expansion proceeds as microtubules are disassembled in the inner region (lagging zone), and new microtubules polymerize at the outer phragmoplast edge (leading zone). Tubulin released in the lagging zone is recycled for the polymerization of new microtubules in the leading zone. Overlapping antiparallel microtubules crosslinked by MAP65 are continuously formed in the leading zone [38]. These overlap regions structurally stabilize the midzone and initiate CPAM formation where the next round of cell plate assembly takes place. Actin filaments are largely polymerized at the leading edge, extending out towards the cell cortex and actively attaching at the CDZ. Myosins on the plus ends of microtubules can interact with the actin meshwork thereby guiding phragmoplast expansion to the division site (as exemplified by myosin VIII in P. patens; [39]). Within the central region of the microtubule ring, formed by the breakdown of microtubules in the central region of the disk phragmoplast and assembly of new microtubules at the leading zone, the growing cell plate becomes a calloserich interconnected tubular network. Remodeling of membrane and cell plate material through clathrin-mediated endocytosis leads to the formation of the planar fenestrated sheet. All stages of cell plate assembly coexist in the expanding phragmoplast. Consequently, the spatiotemporal distribution of individual membrane proteins that contribute to different cell plate assembly processes in the phragmoplast can be different ([25,40]; compare RAB-A2a and KNOLLE in Figure S2). As the phragmoplast often forms off cell center, the attachment of the cell plate to the cell plate fusion site first occurs at one site and then progresses to other sites until the fusion is complete (Figures 1 and S3; [41]). Prior to cell plate attachment, peripheral phragmoplast microtubules at the leading zone interact with the cortex. Then finger-shaped membrane structures (fusion tubes) attach the cell plate to the cell plate fusion site [22,37]. This attachment could be important for stabilizing the position of the cell plate; however, it remains unknown whether attachment site selection within CDZ is stochastic or results from a polarized translocation of the phragmoplast towards a specific position at cell plate fusion site. Microtubules depolymerize at the attachment site, resulting in a discontinuous phragmoplast (Figures 1 and S3). What signals guide the centrifugal expansion remains unknown, but actin filaments have been shown to play a key role in guiding phragmoplast expansion and final positioning of the cell plate. Depolymerization of microtubules following cell plate fusion events results in fragments of phragmoplast scattered along the perimeter of the cell plate fusion site (Figure S3). Upon cell plate fusion, the lumen of the cell plate is continuous with the apoplast and its physicochemical properties subsequently mature into primary cell wall. In addition, the attachment allows diffusion of plasma-membrane proteins and lipids from plasma membrane to the cell plate. These changes trigger a novel phase in cell plate assembly, which has been referred to as cell plate maturation. After attachment, the TRAPPII complex disappears from the cell plate and EXOCYST becomes the predominant tethering complex [24]. This marks a change in trafficking to the cell plate. For example, TPLATE and myosin VIII have been shown to be specifically recruited to the cell plate only after attachment [42,43]. Cell plate maturation results in a cross-wall, which in addition to callose [37,40,44], contains cellulose, hemicellulose, and pectin [45–47]. The cross-wall gradually develops a pectin-rich middle lamella as the cellulose– hemicellulose networks are assembled on the opposite cell plate membranes. However the distinct stages of polysaccharide deposition during cell plate maturation and cross-wall transformation remain to be characterized [6]. Integration of the cross-wall with the [39_TD$IF]parental cell wall involves localized digestion of the cellulose layer of the [39_TD$IF]parental cell wall at the attachment site to enable the middle lamellae of the two walls to form a continuum. The formation of the cross-wall hallmarks completion of the cytokinesis and establishment of the two daughter cells.
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Concluding Remarks
Outstanding Questions
Exciting research of the [367_TD$IF]past decade has not only significantly boosted understanding of plant cytokinesis, but also demonstrated a high degree of complexity of the self-organization processes responsible for both cell plate positioning and formation. The revised terminology aims to capture this complexity and highlights emerging concepts in the plant cytokinesis field. [368_TD$IF]Our work will facilitate addressing the extensive gaps in our knowledge of plant cell cytokinesis (see Outstanding Questions).
How are PPB, ADZ, and cortical division zones spatially and temporarily regulated? How are actin filaments depleted from the ADZ? What changes in membrane proteins and lipids accompany CDZ formation? Do these changes involve interactions with the cell wall?
Acknowledgments Images of dividing BY-2 cells in Figure S3A were taken by Laining Zhang and Deirdre Fahy; images of TAN1 and tubulin were provided by Pablo Martinez. We thank Alex Steiner for support with the assembly of [37_TD$IF]Figure S2 panels. This work was supported by USDA-NIFA hatch grant WNP00826 and WSU startup fund (to AS). EP is supported by the AUTh Research Committee (grant No. [370_TD$IF]91913) by funds of Schur Flexibles Group. CR is supported by NSF-MCB#1505848. IM is supported by BBSRC BB/I022996/1. JŠ is supported by grant No. LO1204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I, MEYS. The authors are grateful to Tobias Baskin, Tijs Ketelaar, and Gohta Goshima for their critical comments on the manuscript. We are also thankful to Bo Liu for encouraging this project.
What factors define microtubule and actin filament organization and trigger their reorganization during phragmoplast expansion? How and to what extent do microtubules and actin filaments need to cooperate to enable correct guidance of the phragmoplast? How does cytokinesis differ between cells that form and do not form a PPB? How do actin filaments guide the phragmoplast expansion?
Supplemental Information Supplemental information associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. tcb.2017.08.008.
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