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ANNUAL
REVIEWS
24 March 2013
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Further
Membrane Microdomains,
Rafts, and Detergent-Resistant
Membranes in Plants
and Fungi
Jan Malinsky,1,, Miroslava Opekarova,2,
Guido Grossmann,3, and Widmar Tanner4,
1
Corresponding authors.
Keywords
lateral plasma membrane compartments, pathogen response,
detergent resistance, sterol-rich domains
Abstract
The existence of specialized microdomains in plasma membranes, postulated for almost 25 years, has been popularized by the concept of
lipid or membrane rafts. The idea that detergent-resistant membranes
are equivalent to lipid rafts, which was generally abandoned after a
decade of vigorous data accumulation, contributed to intense discussions about the validity of the raft concept. The existence of membrane
microdomains, meanwhile, has been veried by unequivocal independent evidence. This review summarizes the current state of research
in plants and fungi with respect to common aspects of both kingdoms.
In these organisms, principally immobile microdomains large enough
for microscopic detection have been visualized. These microdomains
are found in the context of cell-cell interactions (plant symbionts and
pathogens), membrane transport, stress, and polarized growth, and the
data corroborate at least three mechanisms of formation. As documented in this review, modern methods of visualization of lateral membrane compartments are also able to uncover the functional relevance
of membrane microdomains.
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Contents
INTRODUCTION . . . . . . . . . . . . . . . . . .
MEMBRANE MICRODOMAINS
AND LIPID RAFTS: A
HISTORICAL ACCOUNT . . . . . . .
MEMBRANE MICRODOMAINS IN
PLANT AND FUNGAL CELLS:
PHENOMENA AND
POSTULATED FUNCTIONAL
INVOLVEMENT . . . . . . . . . . . . . . . .
Stable Lateral Segregation of
Membrane Transporters . . . . . . . .
Steady-State Microdomains Induced
by Cell Polarization . . . . . . . . . . . . .
Microdomains Induced in Response
to Interaction with
Microorganisms . . . . . . . . . . . . . . . .
FORMATION AND FUNCTIONAL
RELEVANCE OF PLASMA
MEMBRANE MICRODOMAINS
IN PLANTS AND FUNGI . . . . . . . .
Spontaneous Lipid Demixing . . . . . . .
Energy-Dependent Directed
Membrane Flow . . . . . . . . . . . . . . . .
Protein-Mediated Restrictions of
Lateral Diffusion . . . . . . . . . . . . . . . .
Microdomain Organization Needs
Energy: Plasma Membrane of
De-energized Cells . . . . . . . . . . . . .
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INTRODUCTION
The emergence of the plasma membrane
(PM) has been one of the most crucial steps in
evolution. This special organelle surrounding
each cell serves as an active interface between
the cell and its environment. It mediates import
and export of a multitude of molecules with
high selectivity and embeds dozens of sensors
responsible for environmental signal transfer to
the cell interior. In this way, each cell communicates with the environment, and eventually with
neighboring cells and the whole organism. For
a long time, the membrane was imagined as a
uniform envelope made up of lipids and housing
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Malinsky et al.
the proteins responsible for the processes mentioned above. Recent data indicate that the PM
is a highly heterogeneous organelle subdivided
into areas of distinct composition, structure,
and function. These areas were named lipid
or membrane rafts, detergent-resistant membranes (DRMs), micro- or nanodomains, etc.
As discussed below, some of these designations
were unfortunate (see sidebar Essential Terms).
This review summarizes current information about compartments in PMs of plants and
fungi with respect to their size, composition,
dynamics, mechanisms of formation, and functional relevance. Considering the functional
importance of this compartmentation, we focus
on the question of whether it really makes a difference to a cell if a transport or sensor protein
is homogeneously distributed in the membrane
or concentrated at a special location, and what
happens when it is translocated to a different
place within the membrane.
MEMBRANE MICRODOMAINS
AND LIPID RAFTS:
A HISTORICAL ACCOUNT
One important contribution of botany to general biology has been the discovery of the PM
and the phenomenon of osmosis. In plant cells,
which are surrounded by cell walls, plasmolysis could be observed and interpreted in terms
of the existence of a semipermeable membrane
releasing water (but not colored substances like
anthocyanins) from the cell protoplasm (28,
102, 109; reviewed in 129). It was a long time
before this postulated membrane was visualized
by high-resolution electron microscopy (114).
Although modeling of the membrane began
shortly after Gorter & Grendel (38) presented
evidence for the lipid bilayer, the rst generally accepted model (which is still largely accepted today) was Singer & Nicolsons (127)
uid mosaic. The authors modeled cellular membranes as homogeneous lipid bilayers that membrane proteins are either embedded in or attached to, resulting in a mosaic of
protein-containing and bare lipid areas. Postulation of the membrane uidity was based on
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ESSENTIAL TERMS
Membrane microdomain: In the frame of this review, the
terms membrane microdomain and plasma membrane (PM) microdomain denote a lateral compartment within the plane of the
PM that exhibits a composition, structure, and biological function
distinct from the surrounding membrane, regardless of its size,
stability, or mechanism of formation. It is noteworthy that individual membrane microdomains, resulting from spontaneous
and/or energy-dependent lateral segregation of a plentitude of
PM constituents (lipids and proteins), may differ substantially
from one another in all the above-mentioned aspects.
Lipid rafts: Historically, lipid rafts were postulated as Golgi
apparatus or endoplasmic reticulum membranederived sorting platforms forming liquid-ordered microdomains in the PM
that are enriched in sphingolipids and sterols. They are now considered nanoassemblies consisting of specic proteins and lipids.
Membrane microdomains based on lipid rafts are supposed to
be highly dynamic. Their actual size, composition, and function
strongly depend on external conditionstemperature, signaling
events, etc. It is questionable, therefore, whether intact raft-based
microdomains can be detected in isolated membranes.
Detergent-resistant membranes (DRMs): DRMs, also called
detergent-insoluble membranes (DIMs), is a term used for the
nonsolubilized fraction of membranes extracted by mild detergent under dened conditions. Membrane proteins identied as
parts of DRMs are frequently denoted in the literature as raft
proteins, although no relation between the hundreds of proteins
identied in DRMs and their localization in specic membrane
microdomains has been found to date.
importance of lateral membrane compartmentation seems precisely the task of the day.
Differences between particular PM areas
have been repeatedly reported. The polar
accumulation of bacterial chemotaxis receptors is one well-documented example (84).
Another is the acid-banding phenomenon
of internodal cells in Characeae. Zones of
excess proton export alternate with zones of
OH surplus along the long axis of the cell,
which reects different activities of proton
pumps and ion transporters at special PM sites
(82). Differences in membrane composition
are known to exist in polarized cellsfor
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for a subsequent rigorous proof of its associations with a specic membrane structure. This
approach, however, does not address two major concerns. First, proteome analysis of DRM
fractions detects hundreds of proteins (see
Table 1), of which generally very few, if any,
seem to be of special interest for the question
investigated. When employed for protein purication, this approach is therefore rather inefcient compared with other procedures available (afnity chromatography, coimmunoprecipitation, etc.). Second, and an even more serious concern, is that specic associations can
be disrupted by detergents, and protein components that are potentially much more important
in a given study might be discarded solely because they stayed in the detergent-soluble part.
In Saccharomyces cerevisiae, it has been shown
that even cytosolic proteins bind to special
membrane compartments, and these proteins
are, in part, indispensable for the establishment
of these microdomainsfor example, various
eisosomal proteins required for MCC (membrane compartment of Can1) formation (see below as well as References 11, 40, 98, and 151).
The current state of the art in the animal
eldthe guiding example for a long time
does not clarify matters; in fact, in November 2011 Science included the question do lipid
rafts exist? as one of ve cells lingering mysteries that need clarication (75). As pointed
out by Jacobson and coworkers (53), as the accuracy of the experimental approaches was continuously increasing, the sizes of rafts in mammalian cells became smaller and smaller over
time, and are now on the order of <20 nm (30).
This is the magnitude of ordinary protein complexes plus dozens of lipid molecules, in the case
of membrane protein complexes. However, the
raft attributes would then be reduced to functionally relevant interactions of specic proteins with certain lipids. In fact, this has been articulated in a way by Anderson & Jacobson (3) in
their lipid shell hypothesis. In another alternative, Kusumi et al. (68) have suggested a lateral
compartmentation of PMs based on the diffusion of certain proteins in limited membrane
areas; the meshwork of cytoskeletal elements
MCC (membrane
compartment of
Can1): membrane
microdomain in yeast
PMs equivalent to the
furrow-like
invagination supported
by the cytoplasmic
protein complex
(eisosome)
MEMBRANE MICRODOMAINS IN
PLANT AND FUNGAL CELLS:
PHENOMENA AND
POSTULATED FUNCTIONAL
INVOLVEMENT
Stable Lateral Segregation of
Membrane Transporters
Among eukaryotic cells possessing a cell wall,
the rst evidence for clustering of PM constituents or membrane microdomain formation
was obtained in S. cerevisiae. Sur7a membrane protein of unknown function (155)and
the arginine/H+ cotransporter Can1 were observed to localize to discrete spotty zones enriched in ergosterol (40). These zones were
termed the MCC (85). A dozen proteins integral to the PMcomprising several specic
transporters as well as proteins of unknown
functionhave been localized to the MCC
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Malinsky et al.
Gel electrophoresis,
immunoanalysis, MS
Arabidopsis thaliana
Puried PM from seedlings and from
cell culture
Nicotiana tabacum
Puried PM from BY-2 cells
4 reduced, 1 enriched
37 core proteins
14 N/15 N
Arabidopsis thaliana
Puried PM from cell suspension
metabolic labeling,
methyl--cyclodextrin treatment,
quantitative proteomics
Gel electrophoresis, MS
Medicago truncatula
Puried PM from roots
145 enriched
Gel electrophoresis, MS
Nicotiana tabacum
Puried PM from BY-2 cells
Allium porrum
Puried PM from seedlings and from
cell culture
99
15 enriched, 15 depleted
Gel electrophoresis,
immunoanalysis, MS
Arabidopsis thaliana
Total membranes from callus
60
131
(Continued )
74
70
96
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15
108
Reference
Gel electrophoresis,
immunoanalysis-specic antibody,
MS
Lipid analysis
Nicotiana tabacum
Puried PM from leaves and from
BY-2 cells
Protein-detection methods
Gel electrophoresis,
immunoanalysis, freeze-fracture
and immuno-EM
Nicotiana tabacum
Microsomal fraction from leaves
Material
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Table 1
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Gel electrophoresis,
immunoanalysis, MS
Arabidopsis thaliana
Puried PM from seedlings
Abbreviations: EM, electron microscopy; MS, mass spectroscopy; PM, plasma membrane.
a
DRM observed already at early developmental stage.
316 unique
Not identied
Arabidopsis thaliana
Puried PM from suspension cells
Zea mays
Puried PM from embryosa
213 identied
219 identied
Gel electrophoresis,
immunoanalysis, MS
Avena sativa
Puried PM from leaves
95
59
19
137
13
34
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Secale cereale
Puried PM from leaves
Gel electrophoresis,
immunoanalysis, MS
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Oryza sativa
Puried PM from cell suspension
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507
508
Specimen
Probe
Malinsky et al.
Saccharomyces cerevisiae
Arabidopsis thaliana seedling
Arabidopsis thaliana seedling
RICS
ccRICS
TIRFM
VAEM
VA-TIRFM
BiFC
SPT, FCS
FRAP, FRET,
FLIM
Living cells
Protoplasts
FRAP
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
Observation
Uneven protein
distribution
Uneven protein
distribution
Uneven protein
distribution
Composition and
mobility of protein
complexes
Map of protein
mobility
Mobility of proteins
Uneven protein
distribution
Distribution of protein
complexes
Stable higher-order
proteolipid complexes
Mobility of proteins
Mobility of protein
clusters
Uneven protein
distribution
Uneven protein
distribution, mobility
of protein clusters
Uneven protein
distribution
(Continued )
152
64
130
24
36
79
103
65
149
83
136
112
43, 44
66
Reference(s)
24 March 2013
Photoactivation
Native uorescent
proteins (chlorophyll,
phycocyanin,
phycoerythrin)
Living cells
Gloeobacter violaceus
Peptide-specic antibody,
genetically encoded
uorescent proteins
Genetically encoded
uorescent proteins
CLSM
Erratum
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Cells
Solanum tuberosum stem, Solanum
lycopersicum pollen tube
Method
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Pig enterocytes
Living cells
Fixed cells
Saccharomyces cerevisiae
High-pressure-frozen,
freeze-substituted tissue
sections
Adapted PM protein
None
Contrasted product of
enzymatic activity
Peptide-specic antibody
Distribution of protein
clusters
Domains of increased
membrane thickness
Uneven protein
distribution
Uneven protein
distribution
Uneven protein
distribution
Distribution of
protein-specic
membrane
microdomains
Distribution of specic
membrane
microdomains
Distribution of
lipid-specic
microdomains
Distribution of protein
clusters
Distribution of protein
clusters
45
67
77
111
111
71
31
31
30
122, 147
105
Plant references are listed wherever available. Abbreviations: 3D-SIM, three-dimensional structured illumination microscopy; AFM, atomic force microscopy; BiFC, bimolecular uorescence
complementation; ccRICS, cross-correlation raster image correlation spectroscopy; CLSM, confocal laser scanning microscopy; dSTORM, direct stochastic optical reconstruction microscopy;
FCS, uorescence correlation spectroscopy; FLIM, uorescence lifetime imaging; FRAP, uorescence recovery after photobleaching; FRET, Forster
resonance energy transfer; PALM,
photoactivated localization microscopy; RICS, raster image correlation spectroscopy; SPT, single-particle tracking; STED, stimulated emission depletion; TEM, transmission electron
microscopy; TIRFM, total internal reection uorescence microscopy; VAEM, variable-angle epiuorescence microscopy; VA-TIRFM, variable-angle total internal reection uorescence
microscopy.
AFM
Puried PMs
Genetically encoded
uorescent proteins
Glycolipid- and
peptide-specic
antibodies
Callose-specic antibody
Genetically encoded
uorescent proteins
3D-SIM
Fixed cells
STED/FCS
Genetically encoded
uorescent proteins
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Borrelia burgdorferi
STED
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TEM
PALM, dSTORM
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Image restoration:
mathematical method
of increasing image
resolution by
including information
about the imaging
properties of the
microscope; also called
image deconvolution
510
limited uorescence microscopy (72, 85). However, total internal reection uorescence microscopy combined with either image restoration or structured illumination microscopy
(see sidebar Superresolution Fluorescence Microscopy Techniques) has revealed uneven distributions of all PM proteins, including Gap1
and Hxt1, reecting individual and (to various
extents) overlapping microdomains in the PM.
Higher-than-random overlap of four members
of the hexose transporter family possessing
highly similar transmembrane domainsHxt1,
Hxt2, Hxt3, and Hxt6suggests that these microdomains could execute specic functions in
the yeast PM (130).
Immunostaining has revealed accumulation
of the hexose/H+ symporter HUP1 in a punctate pattern in the native PM of Chlorella kessleri.
Interestingly, HUP1 accumulates in the MCC
when functionally expressed in yeast (41). This
observation suggests that lateral microdomains
in yeast PMs could reect an evolutionarily
conserved principle of PM organization. Indeed, specic structures resembling the characteristic furrows of the MCC have been reported in many organisms, including bacteria,
fungi, and plants (134 and references therein).
Krugel
et al. (66) showed that in plant sieve
element cells, the native sucrose transporter
SUT1 also localizes to the PM in a punctate pattern. They suggested that the redox-dependent
dimerization and microdomain association of
SUT1 regulate sugar transport. The potassium
channel KAT1 forms distinct clusters that are
randomly distributed in the PMs of leaf epidermis cells, whereas in guard cells, this channel is ordered in radially oriented linear domains. KAT1 clusters are probably linked to
other cellular structures, as they show a high
degree of positional stability (136). The linear
domains in guard cells depend on turgor pressure, as they disappear under hypertonic conditions. The orientation of KAT1 domains coincides with the orientations of cellulose brils
and the cortical array of microtubules, pointing to an interaction between KAT1 and either the cell wall or the cortical microtubules
(50).
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SUPERRESOLUTION FLUORESCENCE
MICROSCOPY TECHNIQUES
The nite resolution of uorescence microscopy resulting from
the wave nature of light remains a limiting factor in optical detection of membrane microdomains. Therefore, methods breaking the diffraction barrier have become popular in membrane
biology. Membrane microdomains have been successfully resolved by structured illumination microscopy (SIM), stimulated
emission depletion (STED), direct stochastic optical reconstruction microscopy (dSTORM), and photoactivated localization microscopy (PALM). SIM uses excitation by a spatially modulated
beam, which enables reconstruction of high-resolution uorescence signals. In STED, only uorophores in part of the excited
focal volume are allowed to uoresce; the rest are forced to relax
via spectrally distinct stimulated emission. dSTORM and PALM
are stochastic approaches that use iterative light-induced activation of sparse subsets of uorophores, allowing their accurate
localization. This is a time-consuming process, however, which
seriously limits the use of stochastic approaches in vivo.
Superresolution techniques are frequently combined with
total internal reection uorescence microscopy (TIRFM).
Evanescent wave-exciting uorescence in TIRFM penetrates no
further than 200300 nm into the sample, making the use of
TIRFM on membranes covered by a cell wall difcult but not
impossible. A compromise between wide-eld uorescence microscopy and TIRFM in this respect represents variable-angle
epiuorescence microscopy (VAEM) or variable-angle TIRFM
(VA-TIRFM) with adjustable penetration depth.
Flotillins/reggies:
widely expressed and
evolutionarily
conserved proteins
involved in membrane
shaping, pathogenesis,
and symbiotic events
Sterol-rich domains
(SRDs): large,
steady-state PM
microdomains
enriched in sterols,
reecting the dynamic
balance between
directed exocytosis and
lateral diffusion
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Reactive oxygen
species: modulators
of cell wall elasticity
and pathogen defense
that respond to biotic
and abiotic
environmental stimuli
Rac/Rop GTPases:
regulators in plant
signal transduction
that act as molecular
switches, regulating a
variety of processes
such as polarized cell
growth
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LYK3:GFP
FLOT4:mCherry
Merged
LYK3:GFP
FLOT4:mCherry
Merged
2 m
2 m
Figure 1
Redistribution of plant membrane proteins after bacterial treatment. Symbiotic rhizobia trigger a change in the localization of the
Medicago truncatula lysine motif receptor-like kinase LYK3 and the otillin FLOT4. Both proteins accumulate at the root hair cell tips
after bacterial inoculation. In addition, colocalization of LYK3 and FLOT4 increases in inoculated root hairs. (a) Codistributions of
FLOT4:mCherry and LYK3:GFP signals in 3D space. (b) Higher magnication of the images in panel a. Adapted from Reference 44;
c 2011 by the American Society of Plant Biologists.
copyright
Malinsky et al.
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Lipid demixing
Protein scaffolds
Cell wall
Plasma
membrane
Lipids
Cytoskeletal network
Kinetic polarization
Integral protein
Integral protein
Cytoskeletal network
Attached protein
Figure 2
Mechanisms of plasma membrane (PM) microdomain formation. A PM accompanied by a cell wall is shown at various scales. (a) In a
mixture of a large number of different lipids participating in the PM structure (colored circles in panels a and b), one or several specic
lipid species spontaneously aggregate. The resulting nanoscale microdomains exhibit various degree of order. (b) Fast directed vesicular
transport (thick arrow) contributes to microdomain PM organization by forming large, temporary microdomains continuously
dissipated by slow lateral diffusion of the delivered membrane material (thin arrows). (c) Curved membrane domains are supported by
protein scaffolds. For example, furrow-like PM invaginations of the MCC, scaffolded by a hemitubular eisosome, remain apart from
cytoskeletal networks and interfere with the lateral motion of the cortical endoplasmic reticulum. (d ) The PM surface is divided into
small areas by cytoskeletal networks attached to the PM. Proteins attached or integral to the PM, as well as membrane lipids (not
shown), therefore exhibit caged or hop lateral diffusion. Some of the proteins are additionally connected to the cell wall.
normally located in a PM microdomain conveys information about the function of this protein but not about the potential importance of
its localization in a special membrane environment. Just a few casesall in fungal cellsare
currently known where a protein localized in a
specic PM microdomain becomes dislocalized
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Control by change in
location (CCL):
a proposed regulatory
mechanism related to
the compartmentation
of membrane
components and their
induced lateral change
in position
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lipid compositions (Figure 2a) and thus providing individual microenvironments for membrane proteins. For example, in S. cerevisiae,
Pma1 has been shown to prefer an SL-rich
microenvironment (145) but also to avoid the
sterol-rich MCC (85). In addition, independent indications of SL-rich microdomains in
yeast PMs have recently been published (4). Although the distribution of PM SLs has not yet
been shown by direct visualization, these observations indicate at least a partial spatial separation of sterols and SLs in yeast PMs.
It seems evident that the transmembrane domains of integral membrane proteins associate
with specic lipids and that this lipid-protein
interaction determines the protein localization.
Point mutation analysis has shown that a single
transmembrane domain of the plasmodesmatalocated protein PDLP1a determines the
targeting of this membrane protein to plasmodesmata in A. thaliana, and that it can also target
heterologous proteins to this location (141).
Membrane distribution of the yeast ferro-O2 oxidoreductase Fet3, required for iron uptake,
was changed by replacing its transmembrane
domain with the only transmembrane domain
of the small regulatory subunit of the PM
H+ -ATPase Pmp1. The chimera not only
nonrandomly overlapped with Pmp1 but also
lost the Fet3 function. It is unclear whether the
functional defect was caused by protein delocalization from the specic lipid milieu or whether
the transmembrane domain exchange itself
affected the enzymatic activity of the protein.
The MCC-specic arginine permease Can1
has been dislocated to the PM microdomain occupied by the H+ -ATPase Pma1 by direct binding of Can1-GFP to Pma1 tagged with GFP
binder (GB), a monomeric, high-afnity antiGFP antibody. Similarly to Fet3, Can1-GFP
loses its function upon binding to Pma1-GB.
Importantly, however, its transport activity is
preserved when bound to the MCC resident
Sur7-GB, indicating that protein localization
and not the GB binding itself might determine
the effect (130). In wild-type cells, Can1 consistently localizes in the specic ergosterol-rich
lipid milieu of the MCC (40). Furthermore,
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in signal output, especially at low signal intensities, is due to the cooperative association
of interdependent signaling components; this
has been shown, for example, in RAS signaling (142). T cell signaling, however, requires
not raft-based mechanisms but rather direct
protein-protein interactions, which of course
are always a prerequisite for signaling processes
(25). Thus, the specic role of lipid rafts in signaling remains a matter of dispute. In the plant
eld, the importance of rafts in signaling has
been repeatedly stated (102); however, we are
not aware of any convincing evidence for this.
Energy-Dependent Directed
Membrane Flow
For many purposes, including cell growth,
reproduction, sensing, and adaptation to a
wide range of environmental stimuli, the PM is
continuously rearranged. To a large extent, this
membrane ow is accomplished through vesicular transport. The endocytosed membrane can
be directionally recycled to specic sites of the
cell surface (1). This spatial separation of endoand exocytosis, in combination with limited
lateral diffusion of the reinserted membrane
components, is able to maintain steady-state
gradients of PM constituents (Figure 2b).
This was rst demonstrated on peripheral
accumulations of transferrin receptors in the
PMs of human-derived broblasts (17). The
premise of slow lateral diffusion is especially
valid in the PMs of plants and fungi (146).
Therefore, kinetic polarization achieved by
vesicle recycling seems to be a dominant
mechanism of PM domain formation in these
organisms (reviewed in 156).
For example, the formation and maintenance of SRDs in plant and fungal PMs require
a functional secretory pathway. Sterol-rich
membranes of secretory vesicles, routed by
cytoskeletal structures, fuse with the PM at
sites of intensive assembly of the new cell
surface. The spreading of sterol molecules
in the PM is too slow to reach an even
sterol distribution over the cell surface, and a
steady-state sterol gradient is established by
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Protein-Mediated Restrictions
of Lateral Diffusion
The free lateral diffusion of PM constituents
is slowed and obstructed by membraneintegrated or membrane-associated protein assemblies. Based on the mechanisms of their
functions, these assemblies can be categorized as membrane-shaping scaffolds (coats)
(Figures 2c and 4), which generate curvatures in the membrane that represent unique
environments preferred by specic lipid and
protein species, and membrane-cytoskeleton
fences (corrals) (Figure 2d ), which partition
the entire PM into small regions with crossable
borders.
Highly curved areas in biological membranes are usually enriched in specic lipids.
Lipids alone, however, are not likely to generate and maintain this curvature (56). It is, rather,
generated either by membrane-integrated but
not membrane-spanning coat proteins (for
example, caveolins and otillin/reggie proteins; reviewed in Reference 8) or by proteins attached to the cytoplasmic membrane
surface either directly [for example, proteins
containing the BAR (Bin/Amphiphysin/Rvshomology) domain; reviewed in Reference 92]
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100 min
200 min
5
4
3
2
0m
in
20
5 m
10
0m
in
0m
in
PIN1::PIN1-YFP
Polarity index
Figure 3
Mechanism of PIN polarity generation in Arabidopsis roots. (a) The two steps that restore polar plasma
membrane (PM) localization of PIN1-YFP ( rst subpanel ): After complete photobleaching of PIN1-YFP
uorescence (second subpanel ), the newly synthesized protein is rst delivered to the PM in a nonpolar
manner (third subpanel ). Later, polarity is established by spatially conned endocytic recycling ( fourth
subpanel ). Arrowheads point to nonpolar or basal (rootward) PIN1-YFP localization. (b) Ratio of polar to
lateral PIN1-YFP intensity prior to the bleaching (left bar) and at the indicated time points of the recovery of
c 2008 by the
uorescent protein distribution (middle and right bars). Adapted from Reference 23; copyright
Nature Publishing Group.
Pil1/Lsp1
PM
Figure 4
Model for the assembly of yeast eisosomal proteins at the plasma membrane
(PM) in the form of a presumably hemitubular scaffold shaping the furrow-like
membrane invagination of the MCC. Adapted from Reference 58.
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Malinsky et al.
W.B. Frommer & D.W. Ehrhardt, unpublished results) performed uorescence recovery after photobleaching (FRAP)/uorescence
loss induced by photobleaching (FLIP) measurements and particle tracking of individual
protein clusters in Arabidopsis tissue and wallless protoplasts and found that cortical microtubules have a general impact on the dynamics at the PM by dening diffusion barriers and
thereby subdividing the PM into large-scale diffusional domains.
Membrane-associated septins, which are
GTP-binding proteins assembled into rods and
laments in eukaryotic cells from protists to
mammals (but not, however, in higher plants),
partition the PM during cytokinesis (116). In
S. cerevisiae, the septin ring consists of
membrane-anchored circumferential pairs of
tightly associated septin laments interconnected by simple axial laments intersecting the
circumferential laments with 30-nm spacing
(12). During budding, this hourglass-shaped
septin network effectively prevents the mixing
of mother-cell and bud membranes.
In cells possessing cell walls, the mobility of
PM constituents can also be constrained from
the outer PM surface. For example, AtFH1
(A. thaliana actin nucleation protein formin 1)
has been shown to form a bridge across the
PM, connecting the actin cytoskeleton with the
cell wall (90). But even in the absence of direct interactions between PM proteins and cell
wall components, the presence of a cell wall
constrains the lateral diffusion of PM proteins
(91, 103).
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SUMMARY POINTS
1. A large body of evidence supports the existence of membrane microdomains in bacteria,
fungi, and plants. They are mostly stable entities and differ from the highly dynamic lipid
or membrane rafts postulated to exist in mammalian cells.
2. The detergent extraction method does not lead to the isolation of authentic PM microdomains. Use of the differential detergent solubility of membrane proteins has been
a standard purication method, and in this way the procedure may still be useful.
3. Various methods for the direct visualization of membrane microdomains such as superresolution techniques of uorescence microscopy are applicable to plants and should
become the approaches of primary choice in membrane microdomain detection.
4. Several organizing principles result in membrane microdomain formation. Liquidordered phase separation of membrane lipids (lipid rafts) is only one of them.
521
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5. Membrane proteins involved in cell-cell interactions, membrane transport, stress response, and polarized growth have been shown to localize to membrane microdomains.
6. Evidence is available for the functional importance of concentrating specic membrane
components in microdomains. Functional clustering accompanied by modulation of the
activity of PM proteins has been observed, and a new regulatory mechanism is postulated:
control by change in location (CCL).
7. Membrane order, microdomain organization, and general properties like sterol accessibility and detergent susceptibility of the PMs in energized cells differ from those of the
PMs of de-energized or starving cells.
DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
This work was supported by DFG (Priority Program 1108 and TA 36/18-1 to W.T.), Fonds
der Chemischen Industrie (W.T.), grants from the Grant Agency of the Czech Republic
(P302/11/0146 and P205/12/0720 to J.M.), institutional grants (AVOZ 50390703 to J.M. and
RVO 61388971 to M.O.), and an EMBO long-term fellowship (to G.G.).
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Plant Biology
Volume 64, 2013
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