Commentary
1
Structure and function of endosomes in plant cells
Anthony L. Contento and Diane C. Bassham*
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011, USA
*Author for correspondence ([email protected])
Journal of Cell Science
Journal of Cell Science 125, 1–8
ß 2012. Published by The Company of Biologists Ltd
doi: 10.1242/jcs.093559
Summary
Endosomes are a heterogeneous collection of organelles that function in the sorting and delivery of internalized material from the cell
surface and the transport of materials from the Golgi to the lysosome or vacuole. Plant endosomes have some unique features, with an
organization distinct from that of yeast or animal cells. Two clearly defined endosomal compartments have been studied in plant cells,
the trans-Golgi network (equivalent to the early endosome) and the multivesicular body (equivalent to the late endosome), with
additional endosome types (recycling endosome, late prevacuolar compartment) also a possibility. A model has been proposed in which
the trans-Golgi network matures into a multivesicular body, which then fuses with the vacuole to release its cargo. In addition to basic
trafficking functions, endosomes in plant cells are known to function in maintenance of cell polarity by polar localization of hormone
transporters and in signaling pathways after internalization of ligand-bound receptors. These signaling functions are exemplified by the
BRI1 brassinosteroid hormone receptor and by receptors for pathogen elicitors that activate defense responses. After endocytosis of
these receptors from the plasma membrane, endosomes act as a signaling platform, thus playing an essential role in plant growth,
development and defense responses. Here we describe the key features of plant endosomes and their differences from those of other
organisms and discuss the role of these organelles in cell polarity and signaling pathways.
Key words: Endosome, Arabidopsis, Endocytosis
Introduction
The eukaryotic endomembrane system functions in the synthesis,
sorting, delivery and degradation of macromolecules within the
cell. The system is composed of a variety of membrane-bound
organelles that are connected either directly or through a series of
transport vesicles. The main organelles of the endomembrane
system are the endoplasmic reticulum, the Golgi complex and
trans-Golgi network (TGN), endosomes, and lysosomes or
vacuoles. Endosomes have a core sorting function within the
endomembrane system. These organelles are the first point of
fusion for endocytic vesicles, which are used to internalize
extracellular materials. They are also involved in the transport of
materials either from the Golgi to the lysosome or vacuole, or
their return from lysosomes to the Golgi. Endosomes provide
intermediate compartments where materials can be stored, sorted
and then sent to a designated target organelle within the cell
(Anitei et al., 2010; Huotari and Helenius, 2011; Otegui and
Spitzer, 2008).
In plants, lysosomes are generally absent in favor of a large
central vacuole, although there is evidence that lysosome-like
organelles can co-exist with the vacuole in some cells (Takatsuka
et al., 2011). The vacuole is responsible for degradative
functions, in common with lysosomes, and also acts as a large
storage compartment for proteins, water, ions and some defense
compounds (Marty, 1999). Appropriate sorting of proteins at the
TGN is essential for proper maintenance of the central vacuole
and cell wall (Saint-Jore-Dupas et al., 2004). In plants, as in other
organisms, endosomes serve as an entry point for the endocytosis
of external materials and an intermediate compartment in the
transport of macromolecules to the vacuole (Otegui and Spitzer,
2008). However, the organization of the endosomal system in
plants has some unique features when compared with that in
animal cells.
In animal and yeast cells, an array of different types of
endosomes have been identified that can be classified according
to their function during endocytosis. Early endosomes (EEs) are the
first site of deposition of internalized components upon
endocytosis. The internalized components might then be
transported to a recycling endosome for subsequent recycling to
the cell surface, or might enter a multivesicular body (MVB),
designated as an intermediate or late endosome (LE), for transport
to a lysosome or vacuole, often for degradation (Spang, 2009). The
MVB is generally considered to be the point at which endocytic and
biosynthetic vacuolar trafficking meet, and is therefore often also
termed the prevacuolar compartment (PVC) in both yeast and
plants (Gerrard et al., 2000; Tse et al., 2004). A third major
endosome type, the recycling endosome (RE), receives internalized
material from the EE and directs it back to the cell surface or by a
retrograde pathway to the TGN (Hsu and Prekeris, 2010). Although
endosomes perform similar functions of cargo sorting and transport
in plants, they cannot be classified using the same criteria.
Endosomes serve functions beyond the sorting of cargo from
endocytosis and biosynthesis. Plant endosomes are important in
the maintenance of the vacuole and for cell growth, including the
growth of specialized cells such as pollen tubes (Šamaj et al.,
2006; Wang et al., 2010; Richter et al., 2012). The composition
and structure of the plasma membrane and cell wall require
proper endosomal sorting function (Bonifacino and Jackson,
2003; Chow et al., 2008; Toyooka et al., 2009). Endosomes have
also been linked to activation of several signaling pathways (Bar
and Avni, 2009; Geldner et al., 2007; Kang et al., 2010; Robatzek
et al., 2006). Here, we describe the classification and structure of
JCS online publication date 30 August 2012
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Journal of Cell Science
endosomes in plant cells, and discuss how they differ from those
in animal cells. The functions of endosomes in plant cells are
then discussed, with examples of the growing number of
pathways in which they have been found to participate,
including roles in generating cell polarity and in hormonal and
defense signaling.
Endosomal compartments
In animal cells, endosomes have been classified as early
endosomes, which are composed of tubules that are dynamic in
nature; late endosomes (also categorized as multivesicular bodies),
which are typically spherical and contain internal vesicles; and
recycling endosomes, another tubular compartment located close
to the microtubule-organizing center (Huotari and Helenius, 2011).
These compartments can be distinguished by the presence of
specific marker proteins, in particular Rab GTPases (Huotari and
Helenius, 2011). For example, early endosomes might be
detectable by the presence of RAB4 and RAB5, late endosomes
can contain RAB7 or mannose 6-phosphate receptors, and
recycling endosomes contain RAB11. Both early and late
endosomes can recycle their contents back to the plasma
membrane, potentially by a recycling endosome, whereas late
endosomes can either recycle components to the TGN or deliver
them to the lysosome for degradation (Russell et al., 2006).
Transport through the endosomal system in general occurs through
a maturation of endosomes, for example, maturation of an EE into
3
SYP41
SYP42
Ara-4
Pra3
Rab-A2
Rab-A3
SCAMP1
1
RE
a LE by removal of EE-specific components, which is
accompanied by morphological changes in the structure of the
endosome (Huotari and Helenius, 2011).
Although the general functions of endosomes in plant cells are
similar to those in animal cells, the organization of the endosomal
trafficking pathways has some distinct features (see Fig. 1).
Endocytosis has commonly been traced in plant cells using the
fluorescent styryl dye FM4-64 (and related compounds); it labels
the plasma membrane upon addition to intact cells, is taken up by
endocytosis, transported through endosomal compartments and
eventually reaches the vacuolar membrane (Bolte et al., 2004).
Organelles on the endocytic route are therefore sequentially
labeled with fluorescent dye during a time course of uptake.
Various inhibitors that block distinct steps in the endocytic and
endosomal trafficking pathways have allowed the dissection of
trafficking routes and the analysis of proteins potentially
involved in these pathways (see Table 1). To date, there appear
to be two clearly defined and studied endosomal compartments in
plant cells, the TGN or EE and MVB or LE (Fig. 2). Additional
types of endosomes might be present, but their identity awaits
further experimental confirmation.
Early endosomes
EEs are defined as the first compartments that receive endocytic
cargo after internalization from the cell surface, and are labeled
very rapidly by FM4-64 (Bolte et al., 2004). There is now strong
RabA4b
RabA5d
RabA1e
RabA1g
2
TGN
or EE
LE or MVB
or PVC
4
LPVC
GC
1
Nucleus
ER
SYP21
BP80
RabF2a (Rha1)
RabF2b (Ara7)
ESCRT
CHMP1
AtVSRs
Vacuole
Fig. 1. The endocytic pathway in plants. In plants, components of the endocytic pathway are involved in biosynthetic, degradative and recycling transport. The
trans-Golgi network and early endosomes act as the point of organization for these three pathways. This diagram displays the organelles involved in endomembrane
trafficking: nucleus, endoplasmic reticulum (ER), Golgi complex (GC), trans-Golgi network (TGN) or early endosome (EE), late endosome (LE) or multivesicular
body (MVB) or prevacuolar compartment (PVC), late prevacuolar compartment (LPVC), vacuole surrounded by the tonoplast, recycling endosome (RE). The colored
arrows designate potential traffic between organelles. The green arrows indicate pathway 1, the biosynthetic transport route to the plasma membrane that
passes through the TGN and sometimes the MVB. The blue arrow shows a pathway (2) that is taken by plasma membrane components (red ovals) as they are
internalized into endocytic vesicles and move through the TGN. Proteins associated with the TGN are listed (Bassham et al., 2000; Chow et al., 2008; Inaba et al.,
2002; Lam et al., 2007; Sanderfoot et al., 2001; Ueda et al., 1996). The thick, red arrows represent a recycling pathway (3), by which plasma membrane components
might be returned to the plasma membrane through a specialized RE. Proteins associated with the RE are shown (Geldner et al., 2009; Preuss et al., 2006; Rutherford
and Moore, 2002). The orange arrows designate the transport pathway (4) for newly synthesized vacuolar components, as well as cellular materials destined for
degradation in the vacuole. Proteins associated with MVBs are shown (Bottanelli et al., 2012; da Silva Conceição et al., 1997; Jiang and Rogers, 1998; Lee et al.,
2004; Li et al., 2002; Paris et al., 1997; Rutherford and Moore, 2002; Sanderfoot et al., 1998; Sanderfoot et al., 1999; Sohn et al., 2003; Spitzer et al., 2009). Transport
from the TGN to MVBs is designated by a black arrow. Retrograde transport from the VAC to the MVB is represented by curved black arrows.
Endosomes in plants
3
Table 1. Examples of inhibitors used to study endosomal trafficking in plants
Inhibitor
Brefeldin A
Wortmannin
Concanamycin A
Filipin
Journal of Cell Science
Tyrphostin A23
Endosidin1
Effect on plant cells
References
Blocks trafficking from endosomes to plasma membrane
Causes formation of endosomal aggregates (BFA compartment)
Causes redistribution of Golgi proteins to ER
Inhibits PI3K
Causes enlarged PVC/MVB
Inhibits vacuolar ATPase
Blocks transport out of TGN/EE
Prevents vacuolar degradation
Binds plasma membrane sterols
Inhibits endocytosis
Inhibits clathrin-mediated endocytosis
Causes formation of endosomal aggregates
Blocks endocytic trafficking
evidence that, rather than existing as a separate organelle as in
animal cells, in plants, the TGN takes on the function of an early
endosome and is the first site for delivery of endocytosed
material. This was initially proposed by Dettmer and colleagues,
who, using immunogold electron microscopy and fluorescent
labeling, showed that the vacuolar proton–ATPase subunit VHAa1 localizes to the TGN (Dettmer et al., 2006). Surprisingly, the
same marker was also shown to colocalize with FM4-64 very
rapidly after addition of the dye, a hallmark of an EE. Inhibition
(Geldner et al., 2003; Nebenführ et al., 2002; Richter et al., 2007;
Robinson et al., 2008b; Teh and Moore, 2007; Tse et al., 2006)
(Jaillais et al., 2006; Kasai et al., 2011; Matsuoka et al., 1995; Miao
et al., 2006; Tse et al., 2004; Vermeer et al., 2006)
(Dettmer et al., 2006; Matsuoka et al., 1997)
(Grebe et al., 2003; Kleine-Vehn et al., 2006)
(Fujimoto et al., 2010; Ortiz-Zapater et al., 2006)
(Robert et al., 2008)
of the vacuolar ATPase with concanamycin A (Table 1), which
leads to a block in vesicle trafficking, causes the accumulation of
both secretory and endocytic cargo at the TGN (Dettmer et al.,
2006). Endocytosed plasma membrane proteins, secretory
proteins and polysaccharides can all be found in the same TGN
(Viotti et al., 2010), suggesting that these two pathways merged
at this site, now often termed the TGN/EE. Similar results were
obtained using the secretory carrier membrane protein 1
(SCAMP1) protein from rice, which also localized to the TGN
Fig. 2. Use of three-dimensional electron
tomography to distinguish different
regions of the endomembrane system.
(A) Transmission electron microscopy
(TEM) image of a prepared tomographic slice
(4.3 mm thick) through a region of the Golgi
complex and surrounding cytoplasm. Take
note of the division of the Golgi stack from
cis-Golgi (cis) to medial-Golgi (med) to
trans-Golgi (trans) and the trans-Golgi
network (TGN). Specialized labeling
techniques can be used to help distinguish
different cisternae. A non-coated vesicle
(NCV) and a multivesicular body (MVB) are
also labeled. (B) Here, cis-, medial- and
trans-Golgi cisternae seen in A are visualized
as a three-dimensional image, displaying the
divisions of the Golgi stack, as well as a
distinct TGN with associated non-coated and
clathrin-coated vesicles (CCVs). MVBs are
also clearly visible as white bodies attached
to the TGN. (C) Top-down or face-on views
of the Golgi stack. 3D electron tomography
allows for the virtual dissection of the Golgi
stack, from top to bottom (from top, cisternae
are indicated: cis1, cis 2, medial 1, medial 2,
medial 3, trans 2, TGN). The colors for each
cisterna are as in B. This top-down view also
allows visualization of the formation of
protein aggregates (arrows) and CCVs (CC).
Scale bars: 100 nm. Figure reprinted from
Otegui et al. (Otegui et al., 2006)
with permission.
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Journal of Cell Science 125 (0)
and colocalized with FM4-64 at early time points (Lam et al.,
2007), confirming that the previous findings are not dependent on
the TGN marker used.
Evidence exists that the TGN in plants might contain
specialized subdomains with distinct functions. Using
immunogold electron microscopy, TGN marker proteins have
been shown to localize to separate domains of the same TGN
(Bassham et al., 2000). Rab-A2 and Rab-A3 GTPases partially
co-localize with a TGN marker at an organelle that also acts as an
EE (Chow et al., 2008). However, unlike the TGN marker VHAa1, these GTPases are found at the cell plate during cytokinesis,
suggesting that they label an organelle that contributes to
secretory processes (Chow et al., 2008), possibly suggesting
functional differentiation of the TGN or EE during cell division.
Recently, an Arabidopsis mutant lacking a TGN-localized
component was described that is defective in secretory but not
endocytic trafficking, indicating a separation of these two
functions of the TGN (Gendre et al., 2011). Electron
tomography indicates that the TGN is differentiated into early
and late compartments (Kang et al., 2011; Staehelin and Kang,
2008); how these relate to functionally specialized regions is not
yet entirely clear. This differentiation was further analyzed by
live-cell imaging using the secreted protein SCAMP2 as a
marker. SCAMP2 could be seen at the TGN, which was
associated with the Golgi and also could be labeled with FM464, indicating that it was on the endocytic route (Toyooka et al.,
2009). It was subsequently found in a cluster of vesicles derived
from the TGN that contain secretory cargo, including protein and
polysaccharides. This cluster separates from the Golgi, moves to
the plasma membrane, where it fuses and releases its contents
into the cell wall (Toyooka et al., 2009), in a process that possibly
also involves the Rab GTPase ARA6 (Ebine et al., 2011).
Tagging of Golgi and TGN with fluorescent markers followed by
live-cell imaging has demonstrated that the TGN is not
permanently associated with a Golgi stack, but that rather,
individual TGNs move rapidly within the cell and can dissociate
from their associated Golgi and even reassociate with a different
Golgi stack (Viotti et al., 2010). Whether some of these mobile
TGN structures correspond to the secretory clusters described by
Toyooka and co-workers (Toyooka et al., 2009) is unknown.
Late endosomes
Endocytosed material has several possible destinations after
arriving at an EE. It might be recycled back to the plasma
membrane, maintained in the EE as it matures into a LE, or
possibly transported to earlier compartments of the secretory
pathway. Unlike EEs, LEs have a multivesicular structure, in
which the external limiting membrane of the endosome buds
inward to produce internal vesicles. Functionally, this structure
allows delivery of membrane to both the lysosomal or vacuolar
membrane by fusion of the external endosomal membrane with
the lysosomal or vacuolar membrane and to the lumen of the
lysosome or vacuole for degradation in the internal vesicles. It
has therefore been predicted that membrane proteins that are
destined for degradation would be concentrated into the internal
vesicles of LEs, whereas those destined for recycling would
remain on the limiting outer membrane (Babst, 2011).
Evidence that MVBs, which were identified morphologically
by electron microscopy, act as LEs in plants was provided by the
demonstration in tobacco cell culture, by FM4-64 labeling, that
these organelles are on the endocytic pathway (Tse et al., 2004).
MVBs also contain vacuolar sorting receptors and vacuolar
proteins that are en route to the vacuole, suggesting that they are
also intermediates in biosynthetic trafficking to the vacuole
(Bottanelli et al., 2011; Jaillais et al., 2008; Miao et al., 2008; Mo
et al., 2006; Tse et al., 2004). Several Rab GTPases (Ebine et al.,
2011; Ueda et al., 2004; Ueda et al., 2001) were shown to localize
to MVBs and to also colocalize with a PVC marker, but not an
EE or TGN marker, confirming that MVBs observed by electron
microscopy correspond functionally to both a LE and a PVC
(Haas et al., 2007; Miao et al., 2008). Plasma membrane proteins
are found in internal vesicles of MVBs and are absent from the
limiting membrane, indicating that they are en route to the
vacuole for degradation and that recycling to the plasma
membrane must occur from an earlier compartment, either the
TGN or a separate RE (Viotti et al., 2010).
The lumenal vesicles of MVBs are generated through the
endosomal sorting complex required for transport (ESCRT)
machinery. This machinery consists of several protein complexes
(ESCRT-0, -I, -II, -III) that function in the invagination of the
limiting endosomal membrane and release of the vesicles formed,
and in targeting of vacuole-destined plasma membrane proteins
into these vesicles (Henne et al., 2011). Although most of the
ESCRT proteins identified in yeast and animals are conserved in
plants, the ESCRT-0 cargo-sorting complex appears to be
missing in the majority of eukaryotic lineages, including plants
(Leung et al., 2008), and other components might therefore act in
cargo recognition in these organisms, with the Tom1 proteins
being likely candidates based on their interaction with ESCRT
subunits (Richardson et al., 2011). On the basis of protein
localization and the phenotypes of mutants in a few of the plant
ESCRT proteins, in plants, the ESCRT proteins probably
function in LE maturation and sorting of cargo proteins for
degradation (see Fig. 3) (Haas et al., 2007; Ibl et al., 2012;
Katsiarimpa et al., 2011; Scheuring et al., 2011; Shahriari et al.,
2011; Spitzer et al., 2009). An example of regulated transport in
which a normally plasma-membrane-localized protein, the BOR1
boron transporter, is internalized and sorted by the ESCRT
complex in response to environmental conditions has recently
been described (Takano et al., 2005) (see Box 1 for more details),
and additional examples probably exist.
A model for endosome formation and maturation has been
proposed, in which, instead of vesicle transport moving cargo
between endosomes, the TGN matures into a MVB, which then
fuses with the vacuole to release its cargo (Scheuring et al.,
2011). The authors of this study were able to capture MVBs
fusing with the vacuole, suggesting that this transport step does
not involve vesicle trafficking. They also imaged MVBs that are
connected to tubules, which they hypothesized to correspond to
immature MVBs derived from the TGN. In support of their
model, ESCRT components are found distributed on the TGN as
well as on MVBs, and disruption of endosome maturation leads
to increased colocalization of TGN and MVB markers (Scheuring
et al., 2011).
An extension of this model is implicated in work by Foresti
and colleagues, in which a mutant vacuolar-sorting receptor is
shown to accumulate in a compartment that is distinct from the
Golgi, TGN and MVB (Foresti et al., 2010). A soluble vacuolar
marker also accumulates in these structures, which contains
members of the Rab5 family of small GTPases (Bottanelli et al.,
2012; Foresti et al., 2010). These structures are therefore
suggested to be an intermediate compartment, termed the late
Endosomes in plants
machinery, back to earlier compartments before fusion of the
LPVC with the vacuole. The retromer complex is likely to be a
key component in this recycling process, consisting in yeast
of two subcomplexes that function in cargo recognition
and membrane association and deformation, respectively
(Schellmann and Pimpl, 2009). These subcomplexes are
conserved in plants (Oliviusson et al., 2006; Pourcher et al.,
2010) and might function in recycling of vacuolar-sorting
receptors during endosome maturation (Shimada et al., 2006;
Yamazaki et al., 2008; Jaillais et al., 2007). Although the exact
site of recycling of vacuolar-sorting receptors is controversial,
with different localization of the retromer complex reported by
different laboratories (Jaillais et al., 2006; Jaillais et al., 2007;
Kleine-Vehn et al., 2008; Niemes et al., 2010a; Niemes et al.,
2010b; Oliviusson et al., 2006; Phan et al., 2008; Pourcher et al.,
2010; Yamazaki et al., 2008), the general principles of the
endosome maturation model are likely to stand.
2
RE
1
TGN
or EE
LE or MVB
or PVC
3
LPVC
TGN
or EE
GC
1
RE
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2
5
Vacuole
Fig. 3. The AUX and PIN auxin carrier proteins are transported by both
ESCRT-dependent and ESCRT-independent pathways. ESCRT is
essential for the degradation of auxin influx carriers (AUX, red ovals) and
pin-formed auxin efflux carriers (PIN1 or PIN2 proteins, black diamonds), but
not for their recycling back to the plasma membrane (Spitzer et al., 2009).
These auxin transporter proteins are essential for proper growth of the cell and
the determination of cellular polarity. The proper positioning of AUX and
PIN proteins at opposite poles of the cell dictates the flow of auxin through
the cell, and AUX and PIN proteins are internalized by endocytosis and
accumulate at the TGN or EE, as illustrated by the blue arrows (pathway 1).
This pathway is ESCRT dependent. The ESCRT-mediated transport pathway
directs the auxin carrier proteins to the internal vesicles of the MVB, where
they will be eventually transported into the lumen of the vacuole for
degradation. AUX and PIN proteins can also be recycled back to the plasma
membrane as illustrated by the thick red arrows (pathway 2) in an ESCRTindependent pathway. Organelles are depicted as in Fig. 1.
PVC (LPVC), between the MVB and vacuole. It is proposed that
the MVB matures into the LPVC by recycling of vacuolar sorting
receptors, and presumably other components of the trafficking
Box 1. BOR1 borate transporter: an example of
regulated endosomal trafficking
Examples of regulated endocytic trafficking in plants have recently
come to light. One of the better studied is the BOR1 borate
exporter. Boron is an essential element for plants, required for
correct cell wall structure (O’Neill et al., 2004), but an excess of
boron is toxic. BOR1 transports borate into the xylem and
therefore controls the amount of boron in the plant (Noguchi
et al., 1997; Takano et al., 2002). Under boron-limiting conditions,
BOR1 is localized to the plasma membrane, but addition of boron
leads to uptake of BOR1 into endosomes and further transport to
the vacuole (Takano et al., 2005). Study of this protein has
provided insight into the signals required for endosomal transport.
Upon addition of boron, BOR1 is ubiquitylated on K590, and
mutation of this residue blocked MVB sorting for degradation in the
vacuole (Kasai et al., 2011). Because BOR1 is present on internal
vesicles of MVBs (Viotti et al., 2010), this raises the possibility that
ubiquitylation of BOR1 signals its transfer into internal vesicles,
presumably through the ESCRT complex.
Role of endosomes in plants
The primary role of the endosome in all eukaryotes is in
endocytosis. Endocytosis has been studied most extensively in
yeast and mammalian systems, partly because of its association
with a number of diseases (Durieux et al., 2010; Li and Difiglia,
2011; Zhang et al., 2009). In plants, endosomes serve these same
basic functions of uptake of extracellular materials to the interior
of the cell (Meckel et al., 2004), and recycling and maintenance
of plasma membrane receptors (Altenbach and Robatzek, 2007).
In addition, other possible roles for endosomes in plant systems
have also been identified in cell polarity and signaling pathways
(Geldner, 2004; Geldner and Robatzek, 2008).
Plasma membrane maintenance and cell polarity are both
linked to the EE or TGN in plants. Plant cell polarity is important
in maintaining overall plant structure, organogenesis and
tropisms. One family of plant proteins with a role in cell
polarity are PIN proteins, plasma-membrane-localized auxin
efflux carriers that are involved in the transport of the plant
hormone auxin. They are important for determining the direction
and extent of growth of individual cells and therefore for the
maintenance of plant cell polarity (Grunewald and Friml, 2010).
The polar localization and maintenance of PIN family members
is controlled by endocytosis (Dhonukshe et al., 2007) and
transport by both ESCRT-dependent and ESCRT-independent
pathways (Spitzer et al., 2009). Several pathways have been
elucidated that control the maintenance of plasma membrane
polarity (Fig. 3), at least in part through the use of the inhibitors
Brefeldin A, which blocks the cycling of the PIN proteins
through endosomes (Kleine-Vehn et al., 2006), and wortmannin,
which inhibits transport out of endosomes (Jaillais et al., 2006)
(see Table 1). For example, localization of PIN1 involves
the endosome-localized GNOM protein, a guanine nucleotide
exchange factor for an ARF GTPase (Geldner et al., 2003;
Tanaka et al., 2009), or an alternative GNOM-like protein GNL2
in tip-growing cells that undergo rapid cell expansion (Richter
et al., 2012), whereas a separate pathway is responsible for the
internalization of PIN2, which requires GNOM-like 1 (Jaillais
et al., 2006; Pan et al., 2009; Teh and Moore, 2007). The auxin
influx carrier AUX1 is regulated by yet another distinct pathway,
but still requires endosomal trafficking (Du et al., 2011; KleineVehn et al., 2006; Robert et al., 2008). The endosome thus
regulates the location of components in different domains of the
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plasma membrane through endocytosis and recycling, which, in
turn, is essential for plant cell growth and polarity.
Endocytosis and signaling are linked through the need for
maintenance and internalization of plasma membrane receptors,
as well as the role of endosomes as platforms for signaling
pathways (Geldner, 2004; Geldner and Robatzek, 2008). In
addition to more typical signaling cascades that are initiated at
the plasma membrane by membrane-localized receptors, several
examples of signaling pathways that involve endosomes are now
known in plants (Geldner and Robatzek, 2008). Some leucinerich repeat receptor kinases can function in signaling mechanisms
that involve the endosome. Upon extracellular ligand binding, the
ligand–receptor complex is internalized, which in the case of
recognition of flagellin by the flagellin-sensitive 2 (FLS2)
receptor, initiates the defense response (Gómez-Gómez and
Boller, 2000). Mutations in the gene encoding FLS2 that block
endocytosis also impair downstream signaling, indicating that
there is a relationship between these two processes (Robatzek
et al., 2006; Salomon and Robatzek, 2006). Another example is
that of the BRI1 brassinosteroid receptor; although its
internalization is independent of ligand binding, experimental
enhancement of its endosomal localization increases
brassinosteroid signaling, suggesting that signaling occurs
preferentially from endosomes rather than the plasma
membrane (Geldner et al., 2007).
An unusual pathway for initiation of signaling has been
described for the extracellular leucine-rich repeat receptor-like
protein LeEix2 from tomato (Ron and Avni, 2004). This class of
proteins are cell-surface receptors, but lack a functional
cytoplasmic domain, which in most receptors functions in
signaling to downstream components (Kruijt et al., 2005); it is
therefore unclear how the signal is transduced in the absence of
this domain. LeEix2 induces defense responses by binding to the
fungal elicitor ethylene-inducing xylanase (EIX), causing its
internalization to endosomes (Bar and Avni, 2009; Bar et al.,
2009). Inhibitor studies demonstrated that endosomes and
endocytosis are required for LeEix2-mediated initiation of
pathogen defense responses (Sharfman et al., 2011).
Surprisingly, the addition of EIX leads to changes in endosome
mobility, with increased directional movement of endosomes in
the presence of the elicitor (Sharfman et al., 2011). Although the
significance of this movement is not yet understood, the
functional implications of endosome dynamics in the defense
of plants against pathogen attack should prove a fascinating topic
of future study.
Closing remarks and future challenges
In this Commentary, we have discussed the structure of the
endomembrane system in plants, with its two main classes of
endosomes, early endosomes (equivalent to the TGN) and late
endosomes (equivalent to multivesicular bodies or prevacuolar
compartments). The differences between endosome organization
in plants compared with animal cells, and in particular the
additional role of the TGN as an early endosome (Dettmer et al.,
2006), highlight the need to study endosomal structure and
function in plant cells to have a complete understanding of these
important organelles. Recent research into plant endosomes has
focused on the regulation of endosomal trafficking and its
relationship to polarized cell growth (Du and Chong, 2011; Ebine
et al., 2011; Richter et al., 2012), the structure and maturation
pathways of different types of endosomes (Kang et al., 2011;
Scheuring et al., 2011; Viotti et al., 2010), and the
characterization of endosomal proteins such as ESCRT and
retromer components involved in transport and maturation
pathways (Pourcher et al., 2010; Shahriari et al., 2011; Wang
et al., 2010). Future important avenues of research will include
the clarification and further characterization of the pathways and
components for recycling from endosomes to the plasma
membrane (Jaillais et al., 2008; Pan et al., 2009; Richter et al.,
2012) and functional analysis of proteins that are required for
endosomal trafficking and maturation (Niemes et al., 2010b;
Otegui and Spitzer, 2008; Pourcher et al., 2010; Robinson et al.,
2008a). The role of endosomes in signaling pathways is still
limited to a small number of examples in plants (Geldner and
Robatzek, 2008; Gu and Innes, 2011; Kang et al., 2010); it is
likely that this number will increase and our understanding of the
function of endosomes as signaling platforms will grow over
the next few years. As new tools are becoming available for the
analysis of endosomal structure, function and trafficking (see
Table 1 for examples), new avenues of research might be
illuminated, and our understanding of these important organelles
will greatly expand.
Acknowledgements
We thank Marisa Otegui for providing Fig. 2.
Funding
This work was supported by a grant from the National Aeronautics
and Space Administration [grant number NNX09AK78G] to D.C.B.
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