The Dynamic Cell 73

Plant cytokinesis: a tale of membrane traffic and

fusion
Gerd Jürgens*1 , Misoon Park*, Sandra Richter*, Sonja Touihri*, Cornelia Krause*2 , Farid El Kasmi*3 and Ulrike Mayer†
*ZMBP, Developmental Genetics, University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany
†ZMBP, Microscopy, University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany

Abstract
Cytokinesis separates the forming daughter cells. Higher plants have lost the ability to constrict the plasma
membrane (PM) in the division plane. Instead, trans-Golgi network (TGN)-derived membrane vesicles are
targeted to the centre of the division plane and generate, by homotypic fusion, the partitioning membrane
www.biochemsoctrans.org

named cell plate (CP). The CP expands in a centrifugal fashion until its margin fuses with the PM at the
cortical division site. Mutant screens in Arabidopsis have identified a cytokinesis-specific syntaxin named
KNOLLE and an interacting Sec1/Munc18 (SM) protein named KEULE both of which are required for vesicle
fusion during cytokinesis. KNOLLE is only made during M-phase, targeted to the division plane and degraded
in the vacuole at the end of cytokinesis. Here we address mechanisms of KNOLLE trafficking and interaction of
KNOLLE with different soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein (SNAP) receptor
(SNARE) partners and with SM-protein KEULE, ensuring membrane fusion in cytokinesis.

Introduction the plasma membrane (PM), thus physically separating the

Cytokinesis is the final step of cell division, partitioning the
cytoplasm of the dividing cell after the two sets of daughter
chromosomes have moved to opposite poles. In animal and
fungal cells, cytokinesis proceeds from the periphery to the
centre, with a contractile actomyosin ring constricting the
cell in the plane of division. In contrast, flowering plants,
and possibly lower plants as well, lack the gene for myosin
II and fail to form the contractile ring. Plants thus pursue a
different strategy for dividing the cell. They deliver a large
number of membrane vesicles along a dynamic cytoskeletal
Biochemical Society Transactions
two daughter cells.
The present review focuses on membrane traffic and fusion
in cytokinesis. Other aspects of cytokinesis such as dynamics
of cytoskeletal arrays or selection of the cortical division site
have been reviewed recently [1–3] and are not discussed.
Formation of the cell plate: origin of the
membrane material

array, the phragmoplast, to the plane of cell division
(Figure 1A). Initially, these vesicles arrive in the centre of
the division plane where they fuse with one another to form
a new membrane compartment called the cell plate (CP).
Subsequently, through depolymerization of microtubules in
the centre and polymerization of microtubules at its outer
surface, the solid phragmoplast is transformed into a hollow
cylinder and expands towards the periphery of the cell such
that later-arriving vesicles are delivered to the margin of the
growing CP. Eventually, the margin of the CP fuses with
Key words: Arabidopsis, cell plate, cytokinesis, membrane fusion, membrane traffic, soluble
N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE).
Abbreviations: ARF-GEF, adenosine ribosylation factor guanine-nucleotide exchange factor; BFA,
brefeldin A; BIG, BFA-inhibited guanine-nucleotide exchange factor (GEF); CP, cell plate; EE, early
endosome; ER, endoplasmic reticulum; GNL1, GNOM-LIKE1; MVB, multivesicular body; NSF, N-
ethylmaleimide-sensitive factor; PEN1, PENETRATION1; PHP, phragmoplast microtubules; PM,
plasma membrane; SM, Sec1/Munc18; SNARE, soluble NSF attachment protein (SNAP) receptor;
TGN, trans-Golgi network; VAMP, vesicle-associated membrane protein.
1
To whom correspondence should be addressed (email gerd.juergens@zmbp.uni-
tuebingen.de).
2
Present address: Staatliches Museum für Naturkunde Stuttgart, Rosenstein 1, 70191
Stuttgart, Germany
3
Present address: Department of Biology, 4260 Genome Sciences Building, University of
North Carolina, Chapel Hill, NC 27599-3280, U.S.A.
Early electron microscopical studies revealed the accumu-
lation of membrane vesicles in the plane of cell division
(e.g. [4,5]). More studies by Staehelin and colleagues
used electron tomography to describe the dynamics and
quantitative changes in membrane material accumulation
during CP formation [6–9]. Large amounts of membrane
material have to be delivered within a narrow period of
time comprising approximately 30 min in Arabidopsis. Where
does the material come from? The common view was
that the vesicles are derived from Golgi stacks/trans-Golgi
network (TGN), implying that newly synthesized proteins
are delivered to the plane of cell division via a secretory
pathway [6,10] (Figure 1B). However, unbeknownst at that
time, the TGN also receives membrane material from the PM
via endocytosis [11,12]. Endocytosis was then proposed as an
alternative source of CP material [13], which received quite
some publicity, presumably because recycling of endocytosed
material had been shown to play a role in animal cytokinesis
[14,15].
Endocytosis and recycling in interphase seem to be a
general feature of PM proteins in Arabidopsis. Whereas
recycling can be inhibited by the fungal toxin brefeldin
A (BFA), secretion and endocytosis are BFA-resistant in

Biochem. Soc. Trans. (2015) 43, 73–78; doi:10.1042/BST20140246 

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Figure 1 Formation of the cell plate during plant cytokinesis

(A) Dynamics of membrane fusion. Membrane vesicles delivered along PHPs to the plane of cell division fuse with one
another to form the CP. This process starts in the centre and progresses centrifugally, resulting in lateral expansion of the CP
(arrows). DN, forming daughter nuclei. (B) Trafficking pathways during cytokinesis. Both newly synthesized (blue arrows)
and endocytosed (red arrows) proteins are delivered via TGN/EE to the plane of cell division. In contrast, secretory trafficking
and endosomal recycling to the PM are strongly diminished if not abolished (dotted arrows).

Arabidopsis [16–21]. BFA targets the vesicle-budding regu-
lators named ADP-ribosylation factor guanine-nucleotide-
exchange factors (ARF-GEFs), which can be either BFA-
sensitive or resistant, depending on specific amino-acid
residues in their catalytic domain. In contrast with many
other organism including most plant species, yeast, animals
and human cells, the regulation of the secretory pathway
involves BFA-resistant ARF-GEFs in Arabidopsis. GNOM
(BFA-sensitive) and GNL1 (BFA-resistant) jointly regulate
Golgi-ER traffic, whereas BFA-inhibited guanine-nucleotide
exchange factor 1–4 (BIG1–BIG4) (BIG1, BIG2 and BIG4
are BFA-sensitive; BIG3 is BFA-resistant) mediate TGN-
PM trafficking. In contrast, GNOM alone regulates the BFA-
sensitive recycling pathway from endosomes to the basal PM.
BFA treatment of dividing tobacco BY-2 cells arrested
cytokinesis, which was taken as evidence that secretion of
newly synthesized proteins was essential for cytokinesis
[10,22]. How many and which proteins had to be made
de novo remained unclear. In Arabidopsis, syntaxin (also
known as Qa-SNARE) KNOLLE had been known to play
an essential role in cytokinesis and to be present in the cell
during mitosis and cytokinesis only [23,24]. Furthermore,
KNOLLE initially accumulates at the Golgi stacks/TGN
before being directly delivered to the plane of cell division
and is targeted, via the multivesicular bodies (MVBs), to
the vacuole for degradation at the end of cytokinesis [25]
(Figure 1B). Inhibiting ER-Golgi traffic, which required
BFA treatment of gnl1 mutant seedlings to inactivate the
functionally redundant BFA-sensitive ARF-GEF GNOM,
retained KNOLLE in the ER, resulting in binucleate cells,
whereas inhibition of endocytosis by treatment with the
phosphoinositide 3-kinase (PI3K) inhibitor wortmannin had
no effect on cytokinesis [25]. In a subsequent study, a
KNOLLE-related SYP1 syntaxin named PEN1 (also known
as SYP121) was shown to cycle rapidly between the PM and
endosomes and also to accumulate at the plane of cell division
during cytokinesis [26]. Although PEN1 cannot substitute
for KNOLLE when expressed like KNOLLE, a chimeric
PEN1 protein containing the soluble N-ethylmaleimide-
sensitive factor (NSF)-attachment protein (SNAP) receptor
(SNARE) domain of KNOLLE in place of its own can do so.
Interestingly, this chimera only rescued the knolle mutant
when newly synthesized during M-phase, but not when
expressed during S-phase, being delivered to the plane of cell
division in cytokinesis only after endocytosis from the PM
[26]. Thus, in order to have syntaxin activity in cytokinesis,
the protein needs to be delivered along the secretory pathway
directly to the site of action: the CP.
As mentioned above, the TGN/early endosome is at
the crossroads of secretory and endocytic traffic [11,12].
Recently, BIG1–BIG4 have been identified as functionally
redundant ARF-GEFs that mediate late secretion by acting
at the TGN [20]. Interestingly, these ARF-GEFs are not
required for endosomal recycling to the PM, as has most
clearly been demonstrated for trafficking of auxin-efflux
transporter PIN1. Inactivation of BIG1–BIG4 only inhibits
secretion of newly synthesized PIN1 to the PM, whereas
recycling of endocytosed PIN1 is not affected. Conversely,
inactivation of ARF-GEF GNOM inhibits polar recycling
of PIN1, but not overall non-directional secretion of newly


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synthesized PIN1 to the PM [20]. Thus late secretion of
newly synthesized proteins and recycling of endocytosed
proteins are two distinct pathways from the TGN to the
PM in interphase.
Inactivation of secretory ARF-GEFs BIG1–BIG4 disrupts
cytokinesis, resulting in binucleate cells [20]. The same
defect is caused by elimination of the μ-subunit AP1M of
the adaptor protein complex 1 [27,28]. Furthermore, ARF-
GEFs BIG1–BIG4 mediate membrane association of the AP1
complex [20]. Thus AP1-coated vesicles appear to deliver
membrane material to the plane of cell division in plant
cytokinesis.
In contrast with the situation in interphase, inactivation
of BIG1–BIG4 inhibits targeting of both newly synthesized
and endocytosed proteins to the plane of cell division, which
might explain why recycling of most endocytosed proteins to
the PM is largely shut off during cytokinesis [20] (Figure 1B).
There is one exception, however. Polar recycling of PIN1
to the basal PM appears to occur at the same time as
PIN1 targeting to the plane of cell division. This exceptional
case might be explained by the importance of polar auxin
flow for the maintenance of tissue polarity, which otherwise
would be disrupted by the occurrence of many dividing cells
in a developing organ such as the lateral root primordium.
Formation of the cell plate: homotypic
membrane fusion
Golgi/TGN-derived membrane vesicles delivered to the
plane of cell division initially fuse with one another to form
a membranous mesh named CP. Thus membrane fusion
in cytokinesis resembles homotypic fusion, i.e. fusion of
like membranes, and thus is different from heterotypic
fusion in which membrane vesicles fuse with a specific
target membrane that differs in composition from the donor
compartment from which the vesicles budded off. Even at
a later stage of cytokinesis when the CP expands laterally
by fusion of membrane vesicles with its outer margin, the CP
might still resemble the later-arriving vesicles in composition.
Membrane fusion is brought about by complexes of
interacting SNARE proteins and their regulators called
Sec1/Munc18 (SM) proteins [29,30]. Most SNARE proteins
are tail-anchored in the opposing membranes and bear so-
called SNARE domains that form energetically favoured
four-helical bundles mediating membrane fusion. SNARE
proteins fall into different classes named after a specific
amino-acid residue in the centre of the SNARE domain:
Qa-SNAREs (also known as syntaxins), Qb-SNAREs, Qc-
SNAREs and R-SNAREs. In addition, a particular Qbc-
SNARE class comprises proteins with two SNARE domains.
A complex is made up of one member of each class Qa, Qb,
Qc and R-SNAREs; alternatively, Qa, Qbc and R-SNAREs
form a complex. Whereas the former type of complex forms
on endomembranes the latter type has been described for
PM-localized complexes [31–34].
The Dynamic Cell 75
A genetic screen for mutants displaying abnormal body
pattern at the seedling stage provided an entry point into the
analysis of cytokinesis in Arabidopsis, yielding mutant alleles
of two genes specifically required for cytokinesis: KNOLLE,
which encodes a flowering-plant-specific and cytokinesis-
specific syntaxin, and KEULE, which encodes a cytokinesis-
essential SM protein [23,24,35–37]. In essence, knockout
mutations in either gene prevent the fusion of membrane
vesicles with one another in the plane of cell division.
These unfused vesicles persist into interphase and tend to
fuse locally with the PM, giving rise to characteristic cell-
wall stubs. Although the mutant phenotypes appear almost
identical, KNOLLE transcription and mRNA turnover
as well as protein degradation are regulated in a cell
cycle-dependent manner, in contrast with the continual
transcription of KEULE, its mRNA and protein stability
[23,24,37,38].
Domain-swapping experiments involving KNOLLE and
the MVB-localized syntaxin PEP12 have been performed
in order to identify specific regions of KNOLLE protein
required for its biological function in cytokinesis [39].
Only two regions of KNOLLE are critical for syntaxin
function in cytokinesis: the linker 40 amino-acid residues
long between the N-terminal three helices and the SNARE
domain, and the SNARE domain itself. Whereas the latter
mediates interaction with SNARE partners, the linker had not
been assigned any specific role. However, subsequent studies
revealed that the linker sequence is critical for interaction
with the SM-protein KEULE.
Role of SM-protein KEULE in vesicle fusion
during cell-plate formation
SM-proteins have been proposed to facilitate membrane
fusion by interaction with monomeric SNARE proteins
and/or SNARE complexes [29,40]. SM-protein KEULE of
Arabidopsis is most closely related to PM SM-proteins Sec1p
of yeast and mammalian Munc18 [37]. Unlike its homologues,
however, KEULE interacts with the KNOLLE monomer
only and furthermore, with the linker of KNOLLE in
a sequence-specific manner [41]. This specific interaction
requires the open conformation of KNOLLE and only
occurs in the plane of cell division where both proteins
arrive independently: whereas KNOLLE is trafficked from
the ER via the Golgi/TGN, KEULE associates with the
membranes in the plane of cell division directly from the
cytosol [41,42]. These results have led to the following
scenario of how homotypic membrane fusion is brought
about during cytokinesis [41] (Figure 2). Each vesicle arriving
at the plane of cell division carries KNOLLE-containing
cis-SNARE complexes (i.e. SNARE complexes on the same
membrane) that are broken up by the activity of NSF
ATPase as normally occurs upon the fusion of a transport
vesicle with its target membrane. As a consequence, the
monomeric syntaxin would fold back onto itself, adopting
the closed conformation, and would thus be unable to interact

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Figure 2 Regulation of membrane fusion during cytokinesis (model)
Membrane vesicles delivered to the plane of division carry KNOLLE-containing cis-SNARE complexes on their surface. As
these complexes are broken up by NSF ATPase, SM-protein KEULE prevents backfolding of monomeric syntaxin KNOLLE
by stabilizing its open conformation. KNOLLE can thus interact with its SNARE partners on opposing membranes, forming
trans-SNARE complexes required for membrane fusion.
with its SNARE partners again. In cytokinesis, however,
KEULE steps in to keep monomeric KNOLLE in its open
conformation until interaction with its SNARE partners on
adjacent vesicles results in the formation of a trans-SNARE
complex (i.e. SNARE complex on opposing membranes)
mediating vesicle fusion. This model is consistent with the
finding that KNOLLE rendered constitutively open bypasses
the requirement of KEULE for CP formation [41].
Different KNOLLE-containing SNARE
complexes mediate vesicle fusion in
cytokinesis
Two interaction partners of KNOLLE had been identified
by interaction studies: Qbc-SNARE SNAP33 and Qb-
SNARE NPSN11 [43,44]. Unlike knolle mutants, however,
snap33 and npsn11 mutants showed no strong cytokinesis
defect. Although both SNAP33 and NPSN11 interacted
with KNOLLE in co-IP assays, SNAP33 did not interact
with NPSN11 [45]. Thus Qa-SNARE KNOLLE forms two
different SNARE complexes, one including SNAP33 and
the other NPSN11. The missing SNARE partners were
subsequently identified by co-IP as Qc-SNARE SYP71
and either one of two nearly identical R-SNAREs, vesicle-
associated membrane protein (VAMP) 721 and VAMP722
[45]. Consistently, snap33 npsn11 double mutants displayed
very similar vesicle-fusion defects to knolle. Functional
redundancy between the two KNOLLE complexes was

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finally demonstrated by snap33 syp71 also displaying a
knolle-like mutant phenotype, whereas the double mutant
npsn11 syp71, which lacks only one of the two KNOLLE-
containing SNARE complexes, gave no enhanced mutant
phenotype [45]. Thus cytokinesis in Arabidopsis is mediated
by two different KNOLLE-containing SNARE complexes
of which one conforms to the PM type (Qa KNOLLE,
Qbc-SNARE SNAP33, R-SNARE VAMP721/VAMP722),
whereas the other represents the endomembrane type (Qa
KNOLLE, Qb-SNARE NPSN11, Qc-SNARE SYP71, R-
SNARE VAMP721/VAMP722).
Later phases of cytokinesis: expansion of
the cell plate and fusion with the parental
plasma membrane
Membrane fusion and dynamic reorganization of the
phragmoplast microtubules (PHPs) resulting in lateral
translocation drive plant cytokinesis in a centrifugal direction
until the margin of the expanding CP fuses with the parental
PM. Lateral expansion of the CP is accompanied by clathrin-
mediated endocytosis that removes excess membrane material
[8].
How the fusion of the CP margin with the parental PM
is brought about has not been worked out mechanistically.
KNOLLE is endocytosed and targeted to the vacuole
for degradation at the end of cytokinesis [24,25]. This
would leave its SNARE partners SNAP33, NPSN11, SYP71,

VAMP721/VAMP722 free to interact with any of the SYP1
syntaxins located at the PM such as PEN1 (also known
as SYP121), SYP122 and SYP132. The other members
of the SYP1 subfamily SYP123 and SYP124, SYP125
and SYP131 are preferentially expressed in root hairs or
exclusively in pollen [46]. The simplest scenario would be
that VAMP721/VAMP722 on the CP interact with a PM-
localized t-SNARE complex of PEN1, SYP122 or SYP132
with SNAP33 or NPSN11 and SYP71, as is the case in
the fusion of transport vesicles with the PM (e.g. [47,48]).
Alternatively, monomeric syntaxin on the PM might interact
with the cognate SNARE partners present on the margin of
the CP.
Concluding remarks
The functional analysis of membrane trafficking in Ar-
abidopsis cytokinesis as sketched in the present review
has established a conceptual framework that obtains in
flowering plants in general. However, phragmoplast-assisted
CP formation has also been reported to occur in cytokinesis
of lower plants including the green alga Coleochaete
orbicularis [49]. Interestingly, syntaxin KNOLLE, which
plays a highly specific role in Arabidopsis cytokinesis, is
encoded in all flowering-plant genomes sequenced to date,
but not in the genome of the gymnosperm Picea abies, the
lycopod Selaginella moellendorffii or the moss Physcomitrella
patens (C. Krause and G. Jürgens, unpublished work). This
raises two questions. (i) How is membrane fusion during
CP formation and expansion brought about in cytokinesis
of lower plants? (ii) Why did KNOLLE originate during
the transition from gymnosperms to angiosperms and why
are there different KNOLLE complexes? We speculate that
originally any of the PM syntaxins might have participated in
membrane fusion during cytokinesis, much like syntaxin 2 in
mammalian cells [50]. Arguably, KNOLLE, with its tighter
regulation, might have sped up the process of cytokinesis in
the flowering plants.
Funding
This review is based on our primary research that has been funded
by the Deutsche Forschungsgemeinschaft (DFG).
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Received 15 September 2014
doi:10.1042/BST20140246