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Endomembrane trafficking overarching cell plate formation
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ScienceDirect Endomembrane trafficking overarching cell plate formation Joanna Boruc1,2 and Daniel Van Damme1,2 By contrast to other eukaryotic kingdoms, plant cytokinesis is an inside-out process. A coordinated action of cytoskeletal transitions and endomembrane trafficking events builds a novel membrane compartment, the cell plate. Deposition of cell wall polymers transforms the lumen of this membrane compartment into a new cross wall, physically separating the daughter cells. The characterization of tethering complexes acting at discrete phases during cell plate formation and upstream of vesicle fusion events, the presence of modulators directing secretion and recycling during cytokinesis, as well as the identification and temporal recruitment of the endocytic machinery, provides a starting point to dissect the transitions in endomembrane trafficking which shape this process. This review aims to integrate recent findings on endomembrane trafficking events which spatio-temporally act to construct the cell plate. Addresses 1 Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium 2 Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium Corresponding author: Van Damme, Daniel ([email protected])
Current Opinion in Plant Biology 2015, 28:92–98 This review comes from a themed issue on Cell biology
microtubule arrays that initially centrally interdigitate at their plus ends and which are stabilized by microtubulebundling proteins (Figure 1a) [1–4]. Vesicle transport along the phragmoplast microtubules is believed to occur via kinesin motors. Although AtPAKRP2 has been proposed as a candidate to fulfil this task in Arabidopsis [5], its function might, however, not be conserved within the plant kingdom, based on localization data and functional analysis in moss [6,7]. Next to vesicle fusion, membrane recycling from the cell plate via clathrin-mediated endocytosis (CME) shapes it to its final composition [8], but membrane removal by CME is apparently not essential for cell plate expansion [9]. Sequential changes in polysaccharide composition are also hallmarks of cell plate progression (reviewed in [10]). Callose, as the predominant cell plate polysaccharide, has long been proposed to stabilize and aid the expansion of the cell plate tubules (Figure 1c,d) [11,12]. Indeed, mutants and compounds which interfere with callose biosynthesis lead to cytokinesis defects [13–18]. As the defects observed in the absence of callose, however, largely concern anchoring deficiencies following cell plate expansion, callose probably predominantly functions during the transformation of the cell plate into a cross wall, in agreement with its late appearance [17].
Edited by Hiroo Fukuda and Zhenbiao Yang For a complete overview see the Issue and the Editorial Available online 24th October 2015 http://dx.doi.org/10.1016/j.pbi.2015.09.007 1369-5266/# 2015 Elsevier Ltd. All rights reserved.
Introduction Cytokinesis is the final phase of cell division which, via a multi-stage process, physically divides daughter nuclei. In plants, this involves both the biogenesis of a transient membrane compartment as well as its transition into a plasma membrane (PM) and a mature cross wall. This review positions recent findings regarding vesicle trafficking events throughout the different stages of cell plate formation (Figure 1). Actively guided transport and fusion of vesicles at the equator of the cell builds the cell plate. Vesicle guidance occurs via the phragmoplast, which evolves out of the anaphase spindle and consists of two parallel-oriented Current Opinion in Plant Biology 2015, 28:92–98
The hypothesis that cellulose is synthesized only during consolidation of the cell plate [11] was recently challenged. Primary cell wall cellulose synthase (CESA) subunits accumulated together with early cytokinesis markers and were active before the expansion stage (Figure 1b,c) [19]. CESA intensities decreasing at the center of the cell plate during the expansion phase intuitively fit best with cellulose deposition occurring immediately after the recruitment of the CESA complexes to the cell plate. The apparent discrepancy regarding the timing of cellulose deposition and the functional relevance of its early deposition with respect to callose, as well as with cellulose synthesis during cross wall formation, leaves room for further studies.
Initiating cell plate formation The inability of plant cells to constrict their PM necessitates de novo cell plate biogenesis from spatially restricted vesicle fusion events, which are tightly coordinated with cell cycle progression. Both the temporal and spatial restrictions are established by the transition of the anaphase spindle into the phragmoplast, which ensures the spatio-temporal accumulation of cell www.sciencedirect.com
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Figure 1
phragmoplast: cell plate:
(a) formation
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initial fusion
biogenesis
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expanding edge fusion
anchoring
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maturation
plasma membrane
Legend: microtubules early secretory vesicle
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endocytic vesicle cell plate forming vesicle fused vesicles decondensing chromosomes
MVB RAB-A
RAB-A RAB-A
BIG1-BIG4
cell plate nucleus plasma membrane
TVN
TN
CME
TVN
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PFS
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RAB-A
TGN Golgi
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(f)
exocyst KNOLLE TRAPPII endocytosis cellulose callose Current Opinion in Plant Biology
Vesicle trafficking during consecutive stages of cell plate formation. (a) Cell plate initiation stage when TGN-derived late secretory vesicles migrate along the phragmoplast towards the cell equator. In this phase BIG1-BIG4 ARF GEFs are required for trafficking of both endocytosed (yellow arrow) and newly synthesized proteins to the forming cell plate (blue arrow representing targeting of cell plate-forming vesicles). Both EXOCYST and TRAPPII-dependent tethering aid initial vesicle fusion. (b) Continued vesicle fusion facilitated by TRAPPII, RAB-A GTPases and dynaminbased restriction leads to the formation of a tubulovesicular network (TVN). (c) The early cell plate starts to expand by microtubule depolymerization at the center and polymerization at the periphery, directing vesicle fusion at the edges to drive cell plate expansion. Microtubule depolymerization at the center also coincides with maturation of the central part of the cell plate, the TVN cell plate at the center undergoes a morphological change and forms a tubular network (TN). (d) Further membrane remodeling including removal of excess material at the center via clathrin-mediated endocytosis (CME) transforms the TN to a planar fenestrated sheet (PFS). The orange rectangle at the right side of the cell indicates a spot where phragmoplast microtubules were removed for clarity. This is the cortical division zone where CME is likely to cause membrane remodeling before anchoring and recycling and/or degradation of proteins diffusing from the cell plate upon anchoring (yellow arrows with question marks). (e) Upon transformation of the cell plate into a cross wall, daughter cells are separated. (F) Visual representation of the timing of the action of tethering complexes (EXOCYST and TRAPPII, green), SNARE-dependent vesicle fusion (KNOLLE, yellow), endocytosis (CME, red) and polysaccharide deposition (cellulose and callose, blue) throughout the cell plate formation stages. By contrast to TRAPPIIdependent tethering, KNOLLE-syntaxin-dependent fusion and callose deposition, EXOCYST-dependent secretion, CME and cellulose deposition continue following cytokinesis.
plate-forming vesicles. Initial vesicle coalescence and dynamin-mediated restriction creates a dumbbellshaped tubulo-vesicular membrane network (TVN), the early cell plate (Figure 1a,b). SNARE-dependent fusion of cell plate-forming vesicles is preceded by vesicle tethering. SNARE function during cytokinesis, the interplay between the cytokinesis-specific syntaxin KNOLLE [20], the Sec1/Munc18 protein KEULE which stabilizes its open conformation [21] and the other SNARE proteins driving vesicle fusion in complex with KNOLLE, was reviewed recently [22]. Tethering complexes such as EXOCYST [23] and TRAPPII [24,25,26,27] function upstream of SNARE-dependent vesicle fusion and provide spatial www.sciencedirect.com
specificity in concert with RAB-A GTPases [25,28,29]. The EXOCYST tethering complex likely participates in the initiation of cell plate formation due to (1) the prominent association of several subunits during the earliest phases of cell plate formation [23,26,30], (2) the fact that EXOCYST-shaped complexes were observed in electron tomograms connecting unfused vesicles [12] and (3) the formation of aberrantly fused initial cell plate membranes in the exo70A1 mutant [23]. The exact role of the exocyst complex in cell plate initiation remains however unclear as these initial defects are somehow overcome. By contrast to the EXOCYST, the TRAPPII complex labels the cell plate from the onset throughout cytokinesis and is required for its biogenesis [26] (Figure 1f). Current Opinion in Plant Biology 2015, 28:92–98
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Secretory rather than endocytic vesicles drive cell plate biogenesis
As the creation of a novel membrane compartment requires a vast amount of material, the origin of the cell plate forming vesicles has been a longstanding question. Although the convergence of secretory and endocytic pathways at the trans-Golgi network (TGN) in plants [31] is responsible for the early labeling of the forming cell plate with endocytic tracers, evidence has been building up that the secretory rather than the endocytic pathway supplies the bulk of material to construct the cell plate from a RAB-A positive trans-Golgi compartment [28,29,32]. Blocking endoplasmic reticulum to Golgi transport prevents cell plate formation [33–35]. Furthermore, the presence of Golgi-derived pectins in the early cell plates [26] and the observation that endocytosed syntaxin activity is insufficient for cell plate formation [36], strongly corroborate the requirement for de novo secretion for cell plate formation. The late secretory pathway dominates during cytokinesis
Sorting cargo for trafficking depends on the activation of ARF GTPases by their respective guanine-nucleotide exchange factors (ARF-GEF) and the recruitment of adaptor and scaffold proteins to drive vesicle budding. The adaptor protein complex 1 (AP-1) functions at the TGN [37,38] and an AP-1 subunit mutant fails to target KNOLLE to the cell plate [37,39]. Inactivation of the ARF-GEFs BIG1–BIG4, which control secretion from the TGN, impair cell plate formation and mediate AP-1 recruitment to the TGN [40]. Taken together, the above data indicate that AP-1-dependent trafficking contributes extensively to cell plate formation. A longstanding view is that secretion becomes polarized during cytokinesis to ensure sufficient membrane availability to construct the cell plate. Richter and co-workers elegantly showed that this polarization is brought about by recruitment of the majority of endocytosed proteins into the secretory pathway (depending on the ARF-GEFs BIG1–BIG4) at the expense of recycling to the PM (depending on the ARF-GEF GNOM). Trafficking to the cell plate from the TGN is therefore fundamentally different from recycling to the PM [40]. The auxin efflux carrier PIN1 represents a notable exception, as GNOM-dependent basal recycling continues during cytokinesis [40].
From the initial cell plate to cell plate expansion MAPK-dependent depolymerization of microtubules at the center, and polymerization at the edges [41,42], drives phragmoplast expansion and guides vesicle fusion to the rim of the growing cell plate. The centrifugal expansion of the phragmoplast also coincides with the central transition of a TVN to a tubular network (TN, Figure 1c). Current Opinion in Plant Biology 2015, 28:92–98
At the secretory side, TRAPPII, rather than EXOCYSTdependent tethering appears to drive cell plate biogenesis during this stage [26]. By contrast to EXOCYST subunits, TRAPPII subunits label the cell plate throughout cytokinesis and accumulate at its margins. Cell plate accumulation of KNOLLE syntaxin is more defective in trappII mutants in this phase, in contrast to the initial phase of cell plate formation. During cell expansion, trappII mutants also showed patchy and incomplete cell plates [26]. Although dual labeling experiments are lacking, endocytosis of cell plate material likely starts after the initial EXOCYST and TRAPPII accumulation at the cell plate. Indeed, endocytic markers like TPLATE, A/ENTH proteins and clathrin are not visibly recruited to the earliest cell plates and clathrin-coated pits appear at the cell plate expansion stage [9,12,43–45]. The mechanism that controls the onset of endocytosis during cell plate formation remains unknown. The cell plate consists of a high lipid-order and sterol-dependent membrane domain and CME components are enriched in detergent-resistant membrane fractions [46]. The establishment of membrane rafts, ordered assemblies of proteins and sterols, and enriched for long-chain sphingolipids [47], during cell plate formation might therefore be required to initiate endocytosis. Delayed endocytosis from the cell plate was correlated with reduced very long-chain sphingolipid biosynthesis, hinting at a function for these lipids to allow efficient membrane bending required for recycling. Interestingly, reduced sphingolipid content, however, enhanced clathrin recruitment to the early cell plate [44,48]. Our mechanical understanding of CME increased substantially over the last two years with the experimental confirmation of the composition of the plant adaptor protein complex 2 (AP-2) and its function in CME [49,50,51,52,53]. However, while this complex is essential in animal cells [54], loss of AP-2 function in plants only results in mildly aberrant phenotypes [51,52,53]. Next to AP-2, plants possess an eightcore-subunit protein complex (the TPLATE complex, TPC) that acts as the key plant endocytic adaptor complex, as mutations in and/or down-regulation of subunits of the TPC are lethal [55]. In line with a major role for the TPC in plant CME, induced silencing of TPC subunits impaired internalization of several endocytic markers [55]. The TPC complex is claimed to represent an ancient adaptor complex, positioned between coat protein complex I (COPI) and the functional specification of the AP complexes [56]. Moreover, this complex is lost in the lineage leading to animals and fungi [55,56] and plants are likely the only kingdom where this complex retained its pivotal role [57]. Based on available data, the TPC and AP-2 likely function in concert for plant CME, but not exclusively [55]. www.sciencedirect.com
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CME from the cell plate does not function via AP-1 [39] but via the TPC and AP-2 [55]. Although it remains to be unambiguously shown, co-fractionation and co-localization [52] puts two putative RAB-GEFs — Stomatal Cytokinesis Defective 1 and 2 — which cause cytokinesis defects and reduced endocytic tracer uptake from the PM when mutated [4,58], in a likely role of mediating CME from the cell plate in concert with AP-2.
From cell plate expansion to anchoring of the cell plate At this stage, EXOCYST-dependent tethering is reactivated and mediates maturation of the cell plate membrane towards its final PM composition, based on the strong cell plate accumulation of EXOCYST subunits following cell plate anchoring, as well as altered deposition of cell wall polysaccharides in exo84b-2 mutants (Figure 1d) [23,26]. Also, the observation that unattached cell plates occurred in leaf epidermal and guard cells of exo84b mutants [23] and pollen-rescued sec6 mutants [59] supports a role for EXOCYST in cell plate maturation. However, cell plate anchoring and/or cytokinesis defects were not observed in roots of exo84b mutants [26] or in embryos of sec3a mutants [30], while cytokinesis defects were shown in pollen-rescued sec6 mutant embryos [59]. A clear explanation for these differential phenotypes is still missing. Functional redundancy with SEC3B might explain the lack of cytokinesis defects in sec3a mutants and in case of exo84b mutants, it cannot be excluded that certain cell types might be more sensitive to cell plate maturation defects. Novel gene disruption tools such as CRISPR-CAS will no doubt help to solve many observed discrepancies concerning mutant phenotypes, as became possible recently [60]. Hypothetically, exocyst complex subunit composition in plants might also differ at specific intracellular compartments and/or for specific functions, analogous to the discrete AP complexes operating at specific endomembrane locations. Data on exocyst complex composition (e.g. in relation to specific endomembrane compartments, cellular processes and/or in exocyst subunit mutants) would fill this experimental gap. Endocytosis plays a role prior and during cell plate anchoring
Accumulation of TPLATE and TML at the cortical division zone (CDZ) PM domain before cell plate arrival [9,55] and cell plate anchoring defects upon downregulation of TPLATE [61] hint towards a preparatory role for CME leading up to cell plate anchoring. Defective vesicle fusion at the center of the cell plate does allow fusion at the CDZ, creating cell wall stubs [9,33,62], and argues for an alternative vesicle fusion pathway at the end of cytokinesis. Intuitively, this would require a distinct membrane and protein composition at the CDZ specifically promoting fusion in situ. Although direct evidence is www.sciencedirect.com
lacking, the often symmetrical formation of stubs and the requirement of cell plate formation for phragmoplast expansion [35] would argue against microtubule-dependent targeting of these unfused vesicles. Ectopic localization of KNOLLE in a drp1a mutant background and upon TPC subunit silencing or alteration of sterol composition [46,55,63] also suggests a function for CME at the CDZ during cell plate insertion. This is thought to restrict KNOLLE localization to the cell plate [63], but its functional significance remains to be determined. Next to clathrin and TPC subunits [9,55], AP2A1 also localizes at the CDZ during cell plate anchoring in tobacco BY-2 cells (unpublished data), so this is likely not a TPC-specific process, but also involves AP-2. One function of the CDZ-CME might be to remove CESA complexes, as punctae co-labeled with CESA1 and clathrin were shown to bud away from the CDZ [19] and endocytosis of CESA has been hypothesized to be AP-2 dependent [49]. Whether this reflects recycling back to the cell plate as postulated for KNOLLE [63], and why this mechanism would function alongside the centripetal movement of CESA from the parental membrane into the cell plate following anchoring [19] remains to be resolved. The observation that pharmacological inhibition of cell plate recruitment of CME machinery is overcome once the cell plate anchors itself [9], visualizes the differential regulation of membrane trafficking between the expansion and maturation phases of the cell plate, which is plausibly linked to physiological changes upon connecting the cell plate lumen with the apoplastic environment. It is tempting to speculate that the correlation of this endocytic recruitment pathway together with the increased accumulation of EXOCYST subunits represents a final phase in cell plate formation to remodel it to a PM.
Conclusions and future perspectives The microtubule transitions which are hallmarks of plant cytokinesis, have been extensively molecularly dissected (reviewed in [64]). Much alike, endomembrane trafficking during cell plate formation also undergoes various transitions. Dynamic co-localization between tethers, CME markers, as well as callose and cellulose visualization will be necessary to further dissect their relative order during cell plate formation. The identification of two tethering complexes acting at different stages of cell plate formation provide an initial step to start addressing these transitions. Which mechanisms control the timely activity of these tethering factors and does this reflect differential luminal vesicle cargoes? The analysis of cell plate polysaccharide content in tethering factor mutants [26] provides an initial step towards this and although technically very challenging, addressing the luminal cargo and protein content of the Current Opinion in Plant Biology 2015, 28:92–98
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vesicles which are targeted by these tethering complexes represents a major future goal.
6.
A more detailed visualization of cytokinesis defects would allow better characterizing of the reported defects (orientation, stubs, gaps and anchoring) and position them with respect to the different phases of cell plate formation. The present availability of three-dimensional scanning electron microscopy (3D-SEM) [26,65], combined with fluorescence-based detection of cells of interest coupled to a genetically encoded high resolution EM tag [66] will provide three-dimensional ultrastructure and localization and allows the distinguishing of whether incomplete cell plates and cell wall stubs represent true anchoring defects or local gaps, conclusions which are difficult to infer from two-dimensional EM representations or confocal volumes. With respect to this, ultrastructural 3D-SEM analysis of the initial cell plate defects observed in exo70A1 mutants, although technically very challenging, would increase our understanding of the role of the exocyst during the very onset phase of cytokinesis.
7.
Of all cell plate phases, the anchoring of the new cell plate, along with the observation that adjacently dividing cells never form a clean four-way junction [67], remain the most enigmatic. No doubt cell wall modifications are required to allow the new cell wall to be continuous with the existing one. How this works and what needs to be actively endocytosed at this stage remain future challenges.
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Acknowledgements
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Joanna Boruc is supported by a Belgian Science Policy (BELSPO) Back to Belgium postdoctoral fellowship grant (selection year 2012). This work was also supported by a FWO research grant (G029013N). We apologize to all authors whose work could not be included or expanded on due to length restrictions.
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Current Opinion in Plant Biology 2015, 28:92–98
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among plasma-membrane syntaxins in Arabidopsis. Traffic 2011, 12:1269-1280. 37. Park M, Song K, Reichardt I, Kim H, Mayer U, Stierhof YD, Hwang I, Jurgens G: Arabidopsis mu-adaptin subunit AP1M of adaptor protein complex 1 mediates late secretory and vacuolar traffic and is required for growth. Proc Natl Acad Sci U S A 2013, 110:10318-10323. 38. Robinson MS: Adaptable adaptors for coated vesicles. Trends Cell Biol 2004, 14:167-174. 39. Teh OK, Shimono Y, Shirakawa M, Fukao Y, Tamura K, Shimada T, Hara-Nishimura I: The AP-1 mu adaptin is required for KNOLLE localization at the cell plate to mediate cytokinesis in Arabidopsis. Plant Cell Physiol 2013, 54:838-847. 40. Richter S, Kientz M, Brumm S, Nielsen ME, Park M, Gavidia R, Krause C, Voss U, Beckmann H, Mayer U et al.: Delivery of endocytosed proteins to the cell-division plane requires change of pathway from recycling to secretion. Elife 2014, 3:e02131. This manuscript identifies that secretion and recycling pathways, both originating from the TGN in plants, are differentially regulated during interphase and mitosis. Whereas the ARF-GEFs BIG1–4 are not required for recycling endocytosed proteins back to the PM, they are required for the trafficking of endocytosed proteins to the forming cell plate. 41. Nishihama R, Ishikawa M, Araki S, Soyano T, Asada T, Machida Y: The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev 2001, 15:352-363. 42. Nishihama R, Machida Y: Expansion of the phragmoplast during plant cytokinesis: a MAPK pathway may MAP it out. Curr Opin Plant Biol 2001, 4:507-512. 43. Ito E, Fujimoto M, Ebine K, Uemura T, Ueda T, Nakano A: Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging. Plant J 2012, 69:204-216. 44. Molino D, Van der Giessen E, Gissot L, Hematy K, Marion J, Barthelemy J, Bellec Y, Vernhettes S, Satiat-Jeunemaitre B, Galli T et al.: Inhibition of very long acyl chain sphingolipid synthesis modifies membrane dynamics during plant cytokinesis. Biochim Biophys Acta 2014, 1842:1422-1430. 45. Song K, Jang M, Kim SY, Lee G, Lee GJ, Kim DH, Lee Y, Cho W, Hwang I: An A/ENTH domain-containing protein functions as an adaptor for clathrin-coated vesicles on the growing cell plate in Arabidopsis root cells. Plant Physiol 2012, 159:10131025. 46. Frescatada-Rosa M, Stanislas T, Backues SK, Reichardt I, Men S, Boutte Y, Jurgens G, Moritz T, Bednarek SY, Grebe M: High lipid order of Arabidopsis cell-plate membranes mediated by sterol and DYNAMIN-RELATED PROTEIN1A function. Plant J 2014, 80:745-757. 47. Simons K, Sampaio JL: Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 2011, 3:a004697. 48. Bach L, Gissot L, Marion J, Tellier F, Moreau P, SatiatJeunemaitre B, Palauqui JC, Napier JA, Faure JD: Very-longchain fatty acids are required for cell plate formation during cytokinesis in Arabidopsis thaliana. J Cell Sci 2011, 124:32233234. 49. Bashline L, Li S, Anderson CT, Lei L, Gu Y: The endocytosis of cellulose synthase in Arabidopsis is dependent on mu2, a clathrin-mediated endocytosis adaptin. Plant Physiol 2013, 163:150-160. These papers describe the proteomic composition and functional characterization of the evolutionarily conserved AP-2 heterotetrameric endocytic complex in plants. Although mutants in subunits of AP-2 are affected in several aspects of development, loss of single AP-2 subunits is apparently not essential for overall plant viability. 50. Di Rubbo S, Irani NG, Kim SY, Xu ZY, Gadeyne A, Dejonghe W, Vanhoutte I, Persiau G, Eeckhout D, Simon S et al.: The clathrin adaptor complex AP-2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis. Plant Cell 2013, 25:2986-2997. See annotation to Ref. [49]. Current Opinion in Plant Biology 2015, 28:92–98
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51. Fan L, Hao H, Xue Y, Zhang L, Song K, Ding Z, Botella MA, Wang H, Lin J: Dynamic analysis of Arabidopsis AP2 sigma subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 2013, 140:3826-3837. See annotation to Ref. [49]. 52. Yamaoka S, Shimono Y, Shirakawa M, Fukao Y, Kawase T, Hatsugai N, Tamura K, Shimada T, Hara-Nishimura I: Identification and dynamics of Arabidopsis adaptor protein-2 complex and its involvement in floral organ development. Plant Cell 2013, 25:2958-2969. See annotation to Ref. [49]. 53. Kim SY, Xu ZY, Song K, Kim DH, Kang H, Reichardt I, Sohn EJ, Friml J, Juergens G, Hwang I: Adaptor protein complex 2-mediated endocytosis is crucial for male reproductive organ development in Arabidopsis. Plant Cell 2013, 25:2970-2985. See annotation to Ref. [49]. 54. Mitsunari T, Nakatsu F, Shioda N, Love PE, Grinberg A, Bonifacino JS, Ohno H: Clathrin adaptor AP-2 is essential for early embryonal development. Mol Cell Biol 2005, 25:9318-9323. 55. Gadeyne A, Sanchez-Rodriguez C, Vanneste S, Di Rubbo S, Zauber H, Vanneste K, Van Leene J, De Winne N, Eeckhout D, Persiau G et al.: The TPLATE adaptor complex drives clathrinmediated endocytosis in plants. Cell 2014, 156:691-704. Through a combination of protein interactomics, genetics and cell biological approaches, this work identified the existence of a novel adaptor complex which is essential for clathrin-mediated endocytosis (CME) in plants. The TPLATE complex represents an early endocytic module and a unique adaptation of the canonical pathway for CME. 56. Hirst J, Schlacht A, Norcott JP, Traynor D, Bloomfield G, Antrobus R, Kay RR, Dacks JB, Robinson MS: Characterization of TSET, an ancient and widespread membrane trafficking complex. Elife 2014, 3:e02866. Through a structural protein search in 15 eukaryotes and phylogenetic analyses, the authors revealed that the TSET complex, the Dictostelium counterpart of the Arabidopsis TPLATE complex (TPC), represents an evolutionary old adaptor complex which can be positioned in between the emergence of the COPI complex and the differentiation of the AP complexes. The TSET/TPC is completely lost in the lineage leading to human and yeast, although the muniscins, which function as endocytic hubs, are the descendants of the medium subunit of the TSET/TPC.
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57. Zhang Y, Persson S, Hirst J, Robinson MS, van Damme D, Sanchez-Rodriguez C: Change your TPLATE, change your fate: plant CME and beyond. Trends Plant Sci 2015, 20:41-48. 58. Falbel TG, Koch LM, Nadeau JA, Segui-Simarro JM, Sack FD, Bednarek SY: SCD1 is required for cytokinesis and polarized cell expansion in Arabidopsis thaliana [corrected]. Development 2003, 130:4011-4024. 59. Wu J, Tan X, Wu C, Cao K, Li Y, Bao Y: Regulation of cytokinesis by exocyst subunit SEC6 and KEULE in Arabidopsis thaliana. Mol Plant 2013, 6:1863-1876. 60. Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y: Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci U S A 2015, 112:2275-2280. 61. Van Damme D, Coutuer S, De Rycke R, Bouget FY, Inze D, Geelen D: Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 2006, 18:3502-3518. 62. Van Damme D, Inze D, Russinova E: Vesicle trafficking during somatic cytokinesis. Plant Physiol 2008, 147:1544-1552. 63. Boutte Y, Frescatada-Rosa M, Men S, Chow CM, Ebine K, Gustavsson A, Johansson L, Ueda T, Moore I, Jurgens G et al.: Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J 2010, 29:546-558. 64. Lee YR, Liu B: The rise and fall of the phragmoplast microtubule array. Curr Opin Plant Biol 2013, 16:757-763. 65. Kremer A, Lippens S, Bartunkova S, Asselbergh B, Blanpain C, Fendrych M, Goossens A, Holt M, Janssens S, Krols M et al.: Developing 3D SEM in a broad biological context. J Microsc 2015. http://dx.doi:10.1111/jmi.12211. 66. Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK, Sosinsky GE, Ellisman MH, Ting AY: Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat Biotechnol 2012, 30:1143-1148. 67. De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME, Novak O, Yamaguchi N, Yoshida S, Van Isterdael G, Palovaara J et al.: Plant development, Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 2014, 345:1255215.
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ScienceDirect Endomembrane trafficking overarching cell plate formation Joanna Boruc1,2 and Daniel Van Damme1,2 By contrast to other eukaryotic kingdoms, plant cytokinesis is an inside-out process. A coordinated action of cytoskeletal transitions and endomembrane trafficking events builds a novel membrane compartment, the cell plate. Deposition of cell wall polymers transforms the lumen of this membrane compartment into a new cross wall, physically separating the daughter cells. The characterization of tethering complexes acting at discrete phases during cell plate formation and upstream of vesicle fusion events, the presence of modulators directing secretion and recycling during cytokinesis, as well as the identification and temporal recruitment of the endocytic machinery, provides a starting point to dissect the transitions in endomembrane trafficking which shape this process. This review aims to integrate recent findings on endomembrane trafficking events which spatio-temporally act to construct the cell plate. Addresses 1 Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium 2 Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium Corresponding author: Van Damme, Daniel ([email protected])
Current Opinion in Plant Biology 2015, 28:92–98 This review comes from a themed issue on Cell biology
microtubule arrays that initially centrally interdigitate at their plus ends and which are stabilized by microtubulebundling proteins (Figure 1a) [1–4]. Vesicle transport along the phragmoplast microtubules is believed to occur via kinesin motors. Although AtPAKRP2 has been proposed as a candidate to fulfil this task in Arabidopsis [5], its function might, however, not be conserved within the plant kingdom, based on localization data and functional analysis in moss [6,7]. Next to vesicle fusion, membrane recycling from the cell plate via clathrin-mediated endocytosis (CME) shapes it to its final composition [8], but membrane removal by CME is apparently not essential for cell plate expansion [9]. Sequential changes in polysaccharide composition are also hallmarks of cell plate progression (reviewed in [10]). Callose, as the predominant cell plate polysaccharide, has long been proposed to stabilize and aid the expansion of the cell plate tubules (Figure 1c,d) [11,12]. Indeed, mutants and compounds which interfere with callose biosynthesis lead to cytokinesis defects [13–18]. As the defects observed in the absence of callose, however, largely concern anchoring deficiencies following cell plate expansion, callose probably predominantly functions during the transformation of the cell plate into a cross wall, in agreement with its late appearance [17].
Edited by Hiroo Fukuda and Zhenbiao Yang For a complete overview see the Issue and the Editorial Available online 24th October 2015 http://dx.doi.org/10.1016/j.pbi.2015.09.007 1369-5266/# 2015 Elsevier Ltd. All rights reserved.
Introduction Cytokinesis is the final phase of cell division which, via a multi-stage process, physically divides daughter nuclei. In plants, this involves both the biogenesis of a transient membrane compartment as well as its transition into a plasma membrane (PM) and a mature cross wall. This review positions recent findings regarding vesicle trafficking events throughout the different stages of cell plate formation (Figure 1). Actively guided transport and fusion of vesicles at the equator of the cell builds the cell plate. Vesicle guidance occurs via the phragmoplast, which evolves out of the anaphase spindle and consists of two parallel-oriented Current Opinion in Plant Biology 2015, 28:92–98
The hypothesis that cellulose is synthesized only during consolidation of the cell plate [11] was recently challenged. Primary cell wall cellulose synthase (CESA) subunits accumulated together with early cytokinesis markers and were active before the expansion stage (Figure 1b,c) [19]. CESA intensities decreasing at the center of the cell plate during the expansion phase intuitively fit best with cellulose deposition occurring immediately after the recruitment of the CESA complexes to the cell plate. The apparent discrepancy regarding the timing of cellulose deposition and the functional relevance of its early deposition with respect to callose, as well as with cellulose synthesis during cross wall formation, leaves room for further studies.
Initiating cell plate formation The inability of plant cells to constrict their PM necessitates de novo cell plate biogenesis from spatially restricted vesicle fusion events, which are tightly coordinated with cell cycle progression. Both the temporal and spatial restrictions are established by the transition of the anaphase spindle into the phragmoplast, which ensures the spatio-temporal accumulation of cell www.sciencedirect.com
Membrane trafficking during plant cytokinesis Boruc and Van Damme 93
Figure 1
phragmoplast: cell plate:
(a) formation
(b) solid
initial fusion
biogenesis
(c)
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expanding edge fusion
anchoring
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maturation
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Legend: microtubules early secretory vesicle
Vacuole
endocytic vesicle cell plate forming vesicle fused vesicles decondensing chromosomes
MVB RAB-A
RAB-A RAB-A
BIG1-BIG4
cell plate nucleus plasma membrane
TVN
TN
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PFS
? ?
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(f)
exocyst KNOLLE TRAPPII endocytosis cellulose callose Current Opinion in Plant Biology
Vesicle trafficking during consecutive stages of cell plate formation. (a) Cell plate initiation stage when TGN-derived late secretory vesicles migrate along the phragmoplast towards the cell equator. In this phase BIG1-BIG4 ARF GEFs are required for trafficking of both endocytosed (yellow arrow) and newly synthesized proteins to the forming cell plate (blue arrow representing targeting of cell plate-forming vesicles). Both EXOCYST and TRAPPII-dependent tethering aid initial vesicle fusion. (b) Continued vesicle fusion facilitated by TRAPPII, RAB-A GTPases and dynaminbased restriction leads to the formation of a tubulovesicular network (TVN). (c) The early cell plate starts to expand by microtubule depolymerization at the center and polymerization at the periphery, directing vesicle fusion at the edges to drive cell plate expansion. Microtubule depolymerization at the center also coincides with maturation of the central part of the cell plate, the TVN cell plate at the center undergoes a morphological change and forms a tubular network (TN). (d) Further membrane remodeling including removal of excess material at the center via clathrin-mediated endocytosis (CME) transforms the TN to a planar fenestrated sheet (PFS). The orange rectangle at the right side of the cell indicates a spot where phragmoplast microtubules were removed for clarity. This is the cortical division zone where CME is likely to cause membrane remodeling before anchoring and recycling and/or degradation of proteins diffusing from the cell plate upon anchoring (yellow arrows with question marks). (e) Upon transformation of the cell plate into a cross wall, daughter cells are separated. (F) Visual representation of the timing of the action of tethering complexes (EXOCYST and TRAPPII, green), SNARE-dependent vesicle fusion (KNOLLE, yellow), endocytosis (CME, red) and polysaccharide deposition (cellulose and callose, blue) throughout the cell plate formation stages. By contrast to TRAPPIIdependent tethering, KNOLLE-syntaxin-dependent fusion and callose deposition, EXOCYST-dependent secretion, CME and cellulose deposition continue following cytokinesis.
plate-forming vesicles. Initial vesicle coalescence and dynamin-mediated restriction creates a dumbbellshaped tubulo-vesicular membrane network (TVN), the early cell plate (Figure 1a,b). SNARE-dependent fusion of cell plate-forming vesicles is preceded by vesicle tethering. SNARE function during cytokinesis, the interplay between the cytokinesis-specific syntaxin KNOLLE [20], the Sec1/Munc18 protein KEULE which stabilizes its open conformation [21] and the other SNARE proteins driving vesicle fusion in complex with KNOLLE, was reviewed recently [22]. Tethering complexes such as EXOCYST [23] and TRAPPII [24,25,26,27] function upstream of SNARE-dependent vesicle fusion and provide spatial www.sciencedirect.com
specificity in concert with RAB-A GTPases [25,28,29]. The EXOCYST tethering complex likely participates in the initiation of cell plate formation due to (1) the prominent association of several subunits during the earliest phases of cell plate formation [23,26,30], (2) the fact that EXOCYST-shaped complexes were observed in electron tomograms connecting unfused vesicles [12] and (3) the formation of aberrantly fused initial cell plate membranes in the exo70A1 mutant [23]. The exact role of the exocyst complex in cell plate initiation remains however unclear as these initial defects are somehow overcome. By contrast to the EXOCYST, the TRAPPII complex labels the cell plate from the onset throughout cytokinesis and is required for its biogenesis [26] (Figure 1f). Current Opinion in Plant Biology 2015, 28:92–98
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Secretory rather than endocytic vesicles drive cell plate biogenesis
As the creation of a novel membrane compartment requires a vast amount of material, the origin of the cell plate forming vesicles has been a longstanding question. Although the convergence of secretory and endocytic pathways at the trans-Golgi network (TGN) in plants [31] is responsible for the early labeling of the forming cell plate with endocytic tracers, evidence has been building up that the secretory rather than the endocytic pathway supplies the bulk of material to construct the cell plate from a RAB-A positive trans-Golgi compartment [28,29,32]. Blocking endoplasmic reticulum to Golgi transport prevents cell plate formation [33–35]. Furthermore, the presence of Golgi-derived pectins in the early cell plates [26] and the observation that endocytosed syntaxin activity is insufficient for cell plate formation [36], strongly corroborate the requirement for de novo secretion for cell plate formation. The late secretory pathway dominates during cytokinesis
Sorting cargo for trafficking depends on the activation of ARF GTPases by their respective guanine-nucleotide exchange factors (ARF-GEF) and the recruitment of adaptor and scaffold proteins to drive vesicle budding. The adaptor protein complex 1 (AP-1) functions at the TGN [37,38] and an AP-1 subunit mutant fails to target KNOLLE to the cell plate [37,39]. Inactivation of the ARF-GEFs BIG1–BIG4, which control secretion from the TGN, impair cell plate formation and mediate AP-1 recruitment to the TGN [40]. Taken together, the above data indicate that AP-1-dependent trafficking contributes extensively to cell plate formation. A longstanding view is that secretion becomes polarized during cytokinesis to ensure sufficient membrane availability to construct the cell plate. Richter and co-workers elegantly showed that this polarization is brought about by recruitment of the majority of endocytosed proteins into the secretory pathway (depending on the ARF-GEFs BIG1–BIG4) at the expense of recycling to the PM (depending on the ARF-GEF GNOM). Trafficking to the cell plate from the TGN is therefore fundamentally different from recycling to the PM [40]. The auxin efflux carrier PIN1 represents a notable exception, as GNOM-dependent basal recycling continues during cytokinesis [40].
From the initial cell plate to cell plate expansion MAPK-dependent depolymerization of microtubules at the center, and polymerization at the edges [41,42], drives phragmoplast expansion and guides vesicle fusion to the rim of the growing cell plate. The centrifugal expansion of the phragmoplast also coincides with the central transition of a TVN to a tubular network (TN, Figure 1c). Current Opinion in Plant Biology 2015, 28:92–98
At the secretory side, TRAPPII, rather than EXOCYSTdependent tethering appears to drive cell plate biogenesis during this stage [26]. By contrast to EXOCYST subunits, TRAPPII subunits label the cell plate throughout cytokinesis and accumulate at its margins. Cell plate accumulation of KNOLLE syntaxin is more defective in trappII mutants in this phase, in contrast to the initial phase of cell plate formation. During cell expansion, trappII mutants also showed patchy and incomplete cell plates [26]. Although dual labeling experiments are lacking, endocytosis of cell plate material likely starts after the initial EXOCYST and TRAPPII accumulation at the cell plate. Indeed, endocytic markers like TPLATE, A/ENTH proteins and clathrin are not visibly recruited to the earliest cell plates and clathrin-coated pits appear at the cell plate expansion stage [9,12,43–45]. The mechanism that controls the onset of endocytosis during cell plate formation remains unknown. The cell plate consists of a high lipid-order and sterol-dependent membrane domain and CME components are enriched in detergent-resistant membrane fractions [46]. The establishment of membrane rafts, ordered assemblies of proteins and sterols, and enriched for long-chain sphingolipids [47], during cell plate formation might therefore be required to initiate endocytosis. Delayed endocytosis from the cell plate was correlated with reduced very long-chain sphingolipid biosynthesis, hinting at a function for these lipids to allow efficient membrane bending required for recycling. Interestingly, reduced sphingolipid content, however, enhanced clathrin recruitment to the early cell plate [44,48]. Our mechanical understanding of CME increased substantially over the last two years with the experimental confirmation of the composition of the plant adaptor protein complex 2 (AP-2) and its function in CME [49,50,51,52,53]. However, while this complex is essential in animal cells [54], loss of AP-2 function in plants only results in mildly aberrant phenotypes [51,52,53]. Next to AP-2, plants possess an eightcore-subunit protein complex (the TPLATE complex, TPC) that acts as the key plant endocytic adaptor complex, as mutations in and/or down-regulation of subunits of the TPC are lethal [55]. In line with a major role for the TPC in plant CME, induced silencing of TPC subunits impaired internalization of several endocytic markers [55]. The TPC complex is claimed to represent an ancient adaptor complex, positioned between coat protein complex I (COPI) and the functional specification of the AP complexes [56]. Moreover, this complex is lost in the lineage leading to animals and fungi [55,56] and plants are likely the only kingdom where this complex retained its pivotal role [57]. Based on available data, the TPC and AP-2 likely function in concert for plant CME, but not exclusively [55]. www.sciencedirect.com
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CME from the cell plate does not function via AP-1 [39] but via the TPC and AP-2 [55]. Although it remains to be unambiguously shown, co-fractionation and co-localization [52] puts two putative RAB-GEFs — Stomatal Cytokinesis Defective 1 and 2 — which cause cytokinesis defects and reduced endocytic tracer uptake from the PM when mutated [4,58], in a likely role of mediating CME from the cell plate in concert with AP-2.
From cell plate expansion to anchoring of the cell plate At this stage, EXOCYST-dependent tethering is reactivated and mediates maturation of the cell plate membrane towards its final PM composition, based on the strong cell plate accumulation of EXOCYST subunits following cell plate anchoring, as well as altered deposition of cell wall polysaccharides in exo84b-2 mutants (Figure 1d) [23,26]. Also, the observation that unattached cell plates occurred in leaf epidermal and guard cells of exo84b mutants [23] and pollen-rescued sec6 mutants [59] supports a role for EXOCYST in cell plate maturation. However, cell plate anchoring and/or cytokinesis defects were not observed in roots of exo84b mutants [26] or in embryos of sec3a mutants [30], while cytokinesis defects were shown in pollen-rescued sec6 mutant embryos [59]. A clear explanation for these differential phenotypes is still missing. Functional redundancy with SEC3B might explain the lack of cytokinesis defects in sec3a mutants and in case of exo84b mutants, it cannot be excluded that certain cell types might be more sensitive to cell plate maturation defects. Novel gene disruption tools such as CRISPR-CAS will no doubt help to solve many observed discrepancies concerning mutant phenotypes, as became possible recently [60]. Hypothetically, exocyst complex subunit composition in plants might also differ at specific intracellular compartments and/or for specific functions, analogous to the discrete AP complexes operating at specific endomembrane locations. Data on exocyst complex composition (e.g. in relation to specific endomembrane compartments, cellular processes and/or in exocyst subunit mutants) would fill this experimental gap. Endocytosis plays a role prior and during cell plate anchoring
Accumulation of TPLATE and TML at the cortical division zone (CDZ) PM domain before cell plate arrival [9,55] and cell plate anchoring defects upon downregulation of TPLATE [61] hint towards a preparatory role for CME leading up to cell plate anchoring. Defective vesicle fusion at the center of the cell plate does allow fusion at the CDZ, creating cell wall stubs [9,33,62], and argues for an alternative vesicle fusion pathway at the end of cytokinesis. Intuitively, this would require a distinct membrane and protein composition at the CDZ specifically promoting fusion in situ. Although direct evidence is www.sciencedirect.com
lacking, the often symmetrical formation of stubs and the requirement of cell plate formation for phragmoplast expansion [35] would argue against microtubule-dependent targeting of these unfused vesicles. Ectopic localization of KNOLLE in a drp1a mutant background and upon TPC subunit silencing or alteration of sterol composition [46,55,63] also suggests a function for CME at the CDZ during cell plate insertion. This is thought to restrict KNOLLE localization to the cell plate [63], but its functional significance remains to be determined. Next to clathrin and TPC subunits [9,55], AP2A1 also localizes at the CDZ during cell plate anchoring in tobacco BY-2 cells (unpublished data), so this is likely not a TPC-specific process, but also involves AP-2. One function of the CDZ-CME might be to remove CESA complexes, as punctae co-labeled with CESA1 and clathrin were shown to bud away from the CDZ [19] and endocytosis of CESA has been hypothesized to be AP-2 dependent [49]. Whether this reflects recycling back to the cell plate as postulated for KNOLLE [63], and why this mechanism would function alongside the centripetal movement of CESA from the parental membrane into the cell plate following anchoring [19] remains to be resolved. The observation that pharmacological inhibition of cell plate recruitment of CME machinery is overcome once the cell plate anchors itself [9], visualizes the differential regulation of membrane trafficking between the expansion and maturation phases of the cell plate, which is plausibly linked to physiological changes upon connecting the cell plate lumen with the apoplastic environment. It is tempting to speculate that the correlation of this endocytic recruitment pathway together with the increased accumulation of EXOCYST subunits represents a final phase in cell plate formation to remodel it to a PM.
Conclusions and future perspectives The microtubule transitions which are hallmarks of plant cytokinesis, have been extensively molecularly dissected (reviewed in [64]). Much alike, endomembrane trafficking during cell plate formation also undergoes various transitions. Dynamic co-localization between tethers, CME markers, as well as callose and cellulose visualization will be necessary to further dissect their relative order during cell plate formation. The identification of two tethering complexes acting at different stages of cell plate formation provide an initial step to start addressing these transitions. Which mechanisms control the timely activity of these tethering factors and does this reflect differential luminal vesicle cargoes? The analysis of cell plate polysaccharide content in tethering factor mutants [26] provides an initial step towards this and although technically very challenging, addressing the luminal cargo and protein content of the Current Opinion in Plant Biology 2015, 28:92–98
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vesicles which are targeted by these tethering complexes represents a major future goal.
6.
A more detailed visualization of cytokinesis defects would allow better characterizing of the reported defects (orientation, stubs, gaps and anchoring) and position them with respect to the different phases of cell plate formation. The present availability of three-dimensional scanning electron microscopy (3D-SEM) [26,65], combined with fluorescence-based detection of cells of interest coupled to a genetically encoded high resolution EM tag [66] will provide three-dimensional ultrastructure and localization and allows the distinguishing of whether incomplete cell plates and cell wall stubs represent true anchoring defects or local gaps, conclusions which are difficult to infer from two-dimensional EM representations or confocal volumes. With respect to this, ultrastructural 3D-SEM analysis of the initial cell plate defects observed in exo70A1 mutants, although technically very challenging, would increase our understanding of the role of the exocyst during the very onset phase of cytokinesis.
7.
Of all cell plate phases, the anchoring of the new cell plate, along with the observation that adjacently dividing cells never form a clean four-way junction [67], remain the most enigmatic. No doubt cell wall modifications are required to allow the new cell wall to be continuous with the existing one. How this works and what needs to be actively endocytosed at this stage remain future challenges.
Hiwatashi Y, Obara M, Sato Y, Fujita T, Murata T, Hasebe M: Kinesins are indispensable for interdigitation of phragmoplast microtubules in the moss Physcomitrella patens. Plant Cell 2008, 20:3094-3106.
Miki T, Naito H, Nishina M, Goshima G: Endogenous localizome identifies 43 mitotic kinesins in a plant cell. Proc Natl Acad Sci U S A 2014, 111:E1053-E1061. Using endogenous tagging, the authors undertook the daunting task of localizing 72 of the 78 kinesin motor proteins present in the genome of the moss Physcomitrella patens, revealing 43 kinesins functioning during mitosis and most kinesins showing localization patterns which were distinct from the localization of their respective animal homologs. 8.
Otegui MS, Mastronarde DN, Kang BH, Bednarek SY, Staehelin LA: Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 2001, 13:2033-2051.
9.
Van Damme D, Gadeyne A, Vanstraelen M, Inze D, Van Montagu MC, De Jaeger G, Russinova E, Geelen D: Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc Natl Acad Sci U S A 2011, 108:615-620.
10. Drakakaki G: Polysaccharide deposition during cytokinesis: challenges and future perspectives. Plant Sci 2015, 236:177184. 11. Samuels A, Giddings TH Jr, Staehelin LA: Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 1995, 130:1345-1357. 12. Segui-Simarro JM, Austin JR II, White EA, Staehelin LA: Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 2004, 16:836-856. 13. Chen XY, Liu L, Lee E, Han X, Rim Y, Chu H, Kim SW, Sack F, Kim JY: The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiol 2009, 150:105-113.
Acknowledgements
14. Drakakaki G, Robert S, Szatmari AM, Brown MQ, Nagawa S, Van Damme D, Leonard M, Yang Z, Girke T, Schmid SL et al.: Clusters of bioactive compounds target dynamic endomembrane networks in vivo. Proc Natl Acad Sci U S A 2011, 108:1785017855.
Joanna Boruc is supported by a Belgian Science Policy (BELSPO) Back to Belgium postdoctoral fellowship grant (selection year 2012). This work was also supported by a FWO research grant (G029013N). We apologize to all authors whose work could not be included or expanded on due to length restrictions.
15. Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, Kanaoka MM, Hong Z, Torii KU: Dysregulation of cell-tocell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8). Development 2010, 137:1731-1741.
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