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Phragmoplast Expansion: the Four-Stroke Engine That Powers Plant Cytokinesis

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Phragmoplast Expansion: the Four-Stroke Engine That Powers Plant Cytokinesis Available online at www.sciencedirect.com ScienceDirect Phragmoplast expansion: the four-stroke engine that powers plant cytokinesis Andrei Smertenko The phragmoplast is a plant-specific secretory module that postulated in the 19th century by Hofmeister and Le´o partitions daughter cells during cytokinesis by constructing a Errera (reviewed in [4]). In addition to the vasculature, cell plate from membranes and oligosaccharides. The cell plate long divisions also take place during the transition from is typically a long structure, which requires the phragmoplast to 8 to 16 cells in the embryonic stages of Arabidopsis [5]. expand to complete cytokinesis. The phragmoplast expands These long divisions, as well as many other divisions by coordinating microtubule dynamics with membrane throughout plant development, are only possible because trafficking. Each step in phragmoplast expansion involves the plant-specific cytokinetic machinery, termed the phrag- establishment of anti-parallel microtubule overlaps that are moplast, is capable of directional expansion (Figure 1). enriched with the protein MAP65, which recruits cytokinetic vesicles through interaction with the tethering factor, TRAPPII. The backbone of the phragmoplast is made of microtubules Cell plate assembly triggers dissolution of the anti-parallel [6], which function together with microfilaments, mem- overlaps and stabilization of microtubule plus ends through branes, and numerous associated proteins in cell plate assem- association with the cell plate assembly machinery. This bly [7,8]. The phragmoplast is initially positioned between opinion article discusses processes that drive phragmoplast the daughter nuclei during the first round of cell plate expansion as well as highlights key questions that remain for construction (Figure 1a). Once the cell plate begins to mature, better understanding its role in plant cell division. the microtubules depolymerize. At this point, cell plate appears as a tubular network of membrane compartments enriched with callose [8,9]. Depolymerization of the micro- Address tubules is accompanied by the loss of other phragmoplast Institute of Biological Chemistry, College of Human, Agricultural, and components. New microtubules are then polymerized at the Natural Resource Sciences, Washington State University, Pullman, WA 99164, USA edge of the cell plate, which makes phragmoplast appear ring- like [10,11]. Subsequent recruitment of other phragmoplast Corresponding author: Smertenko, Andrei ([email protected]) components initiates the next round of cell plate assembly. Current Opinion in Plant Biology 2018, 46:130–137 Microtubules polymerize at the cell plate edge (phragmo- plast leading zone) and depolymerize at the sites where cell This review comes from a themed issue on Cell biology plate assembly has advanced to the stage of developing the Edited by Elizabeth Haswell and Ram Dixit tubular network (lagging zone; reviewed in [12]). Along the For a complete overview see the Issue and the Editorial longitudinal axis, the phragmoplast comprises all succes- Available online 30th July 2018 sive stages of the nascent cell plate assembly including https://doi.org/10.1016/j.pbi.2018.07.011 vesicles delivery, fusion, oligosaccharide deposition, and membrane remodelling [8]. Observationally, it is clear that 1369-5266/ã 2018 Elsevier Ltd. All rights reserved. the coordination of microtubule dynamics with assembly of the cell plate is a driving force for phragmoplast expansion, though the mechanism(s) behind this coordination remain unknown. Solving complexity of the phragmoplast expan- sion requires mathematical modelling and computer simu- Introduction: phragmoplast expansion lations, however progress toward this goal is slow due to: The colonization of land by plants towards the end of firstly, lack of coherent theoretical model for the phragmo- Silurian period (444–420 mya) launched a new era in the plast expansion; secondly, incomplete list of phragmoplast natural history of Earth, which changed the face of our proteins and gaps in understanding functions of known planet and ultimately resulted in the evolution of phragmoplast proteins; and finally, limited number of humans. The transition of plants from the marine envi- quantification tools and thus numerical parameters of the ronment to the terrestrial one would be impossible with- phragmoplast expansion. This opinion piece summarizes out vascular tissues, which are remarkable in that they are the available data on this topic and addresses the gaps in produced through uncommonly long cell divisions (up to knowledge with speculations on the events in the midzone 1 mm) from cambium meristem cells. What is more, these that comprise the ‘engine’ for phragmoplast expansion. cells divide across their longest axis [1–3]. This phenom- The stages that precede the expansion phase, including enon contrasts divisions that occur in apical meristems, phragmoplast establishment, are reviewed elsewhere which span the shortest cell axis, and breaks the rule [7,11,13]. Current Opinion in Plant Biology 2018, 46:130–137 www.sciencedirect.com The strokes of the phragmoplast expansion engine Smertenko 131 Figure 1 (a) Disk phragmoplast Ring phragmoplast Assembling cell plate Cell plate Nucleus (b) Phragmoplast (c) initiation Phragmoplast expansion DNA Microtubules Distal zones Lagging edge Midzone Midzone μ μ 10 M Leading edge 5 M Current Opinion in Plant Biology Phragmoplast expansion. (a) Completion of cell plate synthesis in the disk phragmoplast triggers depolymerization of microtubules and re- polymerization at the phragmoplast outer edge. Ring phragmoplast continues expansion until it reaches parental cell wall. (b) Phragmoplast expansion in cells expressing GFP-tubulin imaged in the single optical plane using confocal microscope. Phragmoplast vanishes after attachment to the parental cell wall. Midzone remains dark as GFP is excluded from this region. (c) Expanding phragmoplast stained with anti-tubulin (green) and DNA dye DAPI (blue). Phragmoplast midzone lacks staining and appears dark. Stroke 1: establishment of anti-parallel microtubule-associated protein, MAP65, preferably binds microtubule overlaps anti-parallel microtubules that have come into contact The majority of microtubules polymerize inward from the with one-another in the midzone (Figure 2; [18,19]). This phragmoplast distal zones towards the midzone. Conse- finding is complemented by work in vivo, which has quently, microtubules originating from opposing distal shown that several members of the MAP65 gene family zones have reversed polarity: that is, their minus ends accumulate in the phragmoplast midzone [20–23], and orient toward the distal zone, whereas their plus-ends can stabilize microtubules (MAP65-3; [22]) in addition to orient toward the midzone. The establishment of such governing their spatial organization. orientation is supported by both electron microscopy analysis, live-cell imaging, and in silico modelling [14– In animal systems, the anti-parallel microtubule overlaps 17]. In vitro experiments have determined that a can be also recognized by Group 4 kinesins, which can www.sciencedirect.com Current Opinion in Plant Biology 2018, 46:130–137 132 Cell biology Figure 2 Stroke 1 Stroke 2 Stroke 3 Stroke 4 Cell plate assembly matrix Plus end Proteins on the vesicle surface Nasacent cell plate MAP65 Tethering Cytokinetic Plus end factor vesicle Current Opinion in Plant Biology Four stages (strokes) of the phragmoplast expansion. Anti-parallel microtubules from the opposite distal zone are cross-linked by MAP65 in the midzone during Stroke 1. In Stroke 2 MAP65 recruits cytokinetic vesicles to the midzone through interaction with vesicle-tethering factors. Cell plate biogenesis is accompanied by formation of cell plate assembly matrix around nascent cell plate in Stroke 3. At this stage the anti-parallel overlaps disappear and microtubules form attachments to the cell plate assembly matrix. Microtubules depolymerize during Stroke 4 and monomeric tubulin becomes recycled for polymerization of new microtubule in the leading zone. reduce the length of MAP65/PRC1 microtubule overlap [31,32]; however, it is unclear if this phenotype is the in vitro by inhibiting microtubule polymerization [24]. consequence of the cytokinetic function of TRAPPII, or Knockout of MAP65 abrogates cell plate assembly result- its additional role in establishing cell polarity [32]. Sur- ing in multi-nucleated cells and incomplete cell pates in viving TRAPPII mutant plants exhibit fragmented Arabidopsis (cell wall stubs; [25–27]). Conversely, deletion ‘beads-on-the-string’ cell plates in their root apical meri- of two Group 4 kinesins in Physcomitrella patens results in stem [31]. Two subunits of the TRAPPII complex longer anti-parallel microtubule overlap in the phragmo- (TRS130/CLUB and TRS120) were shown to interact plast midzone and in thicker cell plates [28 ]. In addition with MAP65 (isotypes MAP65-1 and MAP65-3) in immu- to Group 4, kinesins from Groups 4, 5, 7, 8, 12, 14 as well noprecipitation and bi-molecular fluorescence comple- as ungrouped kinesins localized to the phragmoplast mentation assays; yeast two-hybrid assay confirmed the midzone (reviewed in [12]). Given ability of some kine- interaction between TRS130 and MAP65-3 [33 ]. sins to slide anti-parallel microtubules, the size of the Hence, binding of TRAPPII to MAP65 constitutes one anti-parallel microtubules overlap could also be regulated mechanism for targeting cell plate vesicles to
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