Nuclear Envelope Disease and Chromatin Organization 2009
The plant nuclear envelope in focus
Katja Graumann and David E. Evans1
School of Life Sciences, Oxford Brookes University, Headington Campus, Oxford OX3 0BP, U.K.
Abstract
Recent progress in understanding the plant NE (nuclear envelope) has resulted from significant advances
in identifying and characterizing the protein constituents of the membranes and nuclear pores. Here, we
review recent findings on the membrane integral and membrane-associated proteins of the key domains
of the NE, the pore domain and inner and outer NEs, together with information on protein targeting and NE
function.
Introduction
The NE (nuclear envelope) is an important but poorly
studied dynamic membrane system in plants. Structurally,
it is similar to those of other kingdoms; however, few of
its functional protein components have been identified so
far. The lack of homologues of well-studied animal and
yeast NE proteins [such as LEM1 (lamin–emerin–man1)
domain proteins, LBR (lamin B receptor), nesprins and
lamins] as well as plant-specific features such as the MT
(microtubule)-nucleating activity of the plant ONM (outer
nuclear membrane) and lack of centrosomes suggest that
knowledge of other organisms cannot be generalized to plants
[1–3]. The present review focuses on current knowledge of
the properties and features of membrane-intrinsic plant NE
proteins as well as their NE targeting mechanisms.
Pore membrane components
Despite the physical continuity of the NE membranes [INM
(inner nuclear membrane), pore membrane and ONM], their
functions and properties differ due to the presence of domainspecific proteins. The pore membrane is a highly curved
membrane that anchors the NPCs (nuclear pore complexes)
to the NE. The composition of animal and yeast NPCs has
been well studied and it has been found that membraneintrinsic nucleoporins such as gp210 and pom121 reside in the
pore membrane and facilitate the anchorage of the NPC [4].
Research on the composition and function of plant NPC is
still in its infancy, and so far only a few functional homologues
of animal and yeast nucleoporins have been characterized
in plants [5–8]. Putative plant homologues of the pore
membrane nucleoporins gp210 and yeast ndc1 (Figure 1)
Key words: Arabidopsis, higher plant, nuclear envelope (NE), nuclear pore complex, Sad1/
UNC-84 (SUN) domain.
Abbreviations used: DMI1, Doesn’t make infection 1; ER, endoplasmic reticulum; GFP, green
fluorescent protein; INM, inner nuclear membrane; KASH, Klarsicht/ANC-1/SYNE homology; LBR,
lamin B receptor; LCA, Lycopersicon calcium ATPase; LEM, lamin–emerin–man; LINC1, little nuclei
1; MAR, matrix attachment region; MT, microtubule; MTOC, MT organizing centres; NE, nuclear
envelope; NLS, nuclear localization signal; NMCP1, nuclear matrix constituent protein 1; NPC,
nuclear pore complex; ONM, outer nuclear membrane; RanGAP, RanGTPase-activating protein;
SPB, spindle pole body; SUN, Sad1/UNC-84, γ -TuRC, γ -tubulin ring complex; WIP, WPP (Try-ProPro) domain-interacting protein; WIT, WPP domain-interacting tail anchored protein.
1
To whom correspondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2010) 38, 307–311; doi:10.1042/BST0380307
have been identified in silico, suggesting similar organization
of the pore membrane and NPC anchorage in plants [9].
In addition, a plant-specific protein family of tail-anchored
membrane proteins have recently been found to be located in
the pore membrane and ONM and to function in RanGAP
(RanGTPase-activating protein) anchorage [10,11]. The role
of the three WIPs [WPP (Try-Pro-Pro) domain-interacting
proteins; WIP1, WIP2a and WIP3] and the two WITs [WPP
domain-interacting tail-anchored proteins; WIT1 and WIT2]
in plant-specific NE targeting mechanisms is discussed
below.
Calcium signalling at the NE
One established function of the plant NE is in calcium
signalling [12]. For instance, perinuclear calcium spiking
in legumes is essential for the formation of symbiotic
relationships causing root nodulation [13,14]. In both animal
and plant cells, the periplasm acts as a Ca2+ store with calcium
channels and pumps located in both INM and ONM involved
in the regulation of nuclear calcium levels independently
of the cytosol [1,12,15]. Downie et al. [16] first reported
the presence of the SERCA (sarcoplasmic/endoplasmic
reticulum Ca2+ -ATPase) type Ca2+ pump homologue LCA
(Lycopersicon calcium ATPase) at the NE in tomato cells.
More recently, it was shown that LCA is located in the
ONM (Figure 1) and functions to replenish the calcium
pool in the NE lumen [15]. Putative INM-localized calcium
channels, including P-type calcium ATPases, nucleotidegated channels and chloride channels, are also predicted to
exist and contribute to nuclear calcium homoeostasis [15].
NE-localized ion channels involved in perinuclear calcium
spiking include the Lotus japonicus homologues CASTOR
and POLLUX and their Medicago truncatula homologue
DMI1 (Doesn’t make infection 1) [13,14,17]. Their
specific functions remain unresolved but it has been
shown that they are permeable to cations [18]. It is
hypothesized that they either act as counter channels allowing
influx of cations into the periplasm in response to Ca2+ efflux
or alter the membrane potential of the NE to open voltagegated Ca2+ channels [18]. It is hypothesized that CASTOR
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Figure 1 Plant NE-intrinsic and -associated proteins
Membrane-intrinsic plant proteins characterized to date include AtSUN1, AtSUN2, LCA, DMI1, CASTOR and POLLUX, as well
as WIPs and WITs. Although γ -TuRC proteins and F-actin (filamentous actin) are associated with the outer surface of the NE,
it is not known what proteins either directly or indirectly tether them there. Likewise, NMCP1, LINC1, LeMFP1 and LeFFPs
associate with the inner side of the NE but their anchoring mechanisms are also unknown. Histone H1 was shown to be
involved in MT nucleation at the ONM but how the nucleoplasmic localized protein is connected to this cytoplasmic event
remains to be established.
is present in the ONM, POLLUX in both ONM and INM
and DMI1 in the INM (Figure 1) because of the presence of
a classical NLS (nuclear localization signal) [13,14,17].
Putative INM components
Proteins of the animal INM have received attention for
their involvement in diseases termed laminopathies [19,20].
This has revealed that in addition to separating nucleoplasm
and cytoplasm, the NE, in particular the INM and its
protein constituents, are actively involved in various nuclear
and cellular processes such as chromatin organization,
transcription, RNA maturation and signalling [19–23].
Interestingly, key players involved in these processes such as
the LBR and LEM domain proteins have no homologues in
plants. Apart from possibly DMI1 and POLLUX, the only
other two putative INM-intrinsic proteins identified so far
are AtSUN1 [Arabidopsis thaliana SUN1 (Sad1/UNC-84)]
and AtSUN2 (Figure 1), putative members of the SUN
domain protein family [3,24]. Originally identified as
homologues of yeast Sad1 [25], we have shown that
the two proteins contain a conserved C-terminal SUN
domain [24] and other conserved features including a
similar domain structure of an N-terminal transmembrane
domain followed by coiled-coil domains as well as
the ability to form heteromers and homomers [24].
Their NE localization and presence of a functional
bipartite NLS suggest that AtSUN1 and AtSUN2 are
components of the plant INM (Figure 1; [24]). In
animals and yeast, SUN domain proteins are part of
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Authors Journal compilation nucleo-cytoskeletal bridging complexes. The INMlocalized SUN domain proteins associate with lamins in the
nucleoplasm and ONM-localized KASH (Klarsicht/ANC-1/
SYNE homology) domain proteins in the periplasm that
interact with cytoskeletal components including actin, SPBs
(spindle pole bodies), MTOCs (MT organizing centres), MT
motor proteins and intermediate filaments [23,26–28]. These
nucleo-cytoskeletal bridging complexes are essential for a
variety of functions including nuclear positioning in the cell,
anchorage of telomeres and decondensation of chromatin
in cell division and apoptotic signalling [21,23,29,30]. The
presence of putative plant SUN domain proteins and the
observation that nuclear histone H1 is involved in MT
organization at the plant ONM (Figure 1) [31] are the only
two indicators that structures similar to the animal and yeast
nucleo-cytoskeletal bridging complexes may also be present
in plants. If they are, however, then their composition and
probably function will differ because plants lack sequence
homologues of lamins and KASH domain proteins and
have different NE–cytoskeletal associations (see below;
[24,32]).
Plant-specific lamin-like elements
In animals, lamins assemble to form a structural lattice
closely associated with the INM that maintains the overall
structure and shape of the nucleus and is involved in various
nuclear processes. Despite the lack of lamin homologues
in plants, recent investigations using field scanning SEM
(scanning electron microscopy) revealed that tobacco nuclei
Nuclear Envelope Disease and Chromatin Organization 2009
also have a filamentous lattice that is similar in structure to
the lamina [33]. It consists of thick and thin filaments and
interconnects NPC. While the identity of the constituents
of the meshwork remains to be established, likely candidates
are plant-specific, nuclear filamentous proteins shown to
localize to the NE periphery (Figure 1). These include the
tomato MAR (matrix attachment region)-binding filamentlike protein 1 (LeMFP1), tomato and Arabidopsis filament-like plant proteins (LeFPPs), carrot NMCP1 (nuclear
matrix constituent protein 1) and its Arabidopsis homologues
LINC1 (little nuclei 1) and LINC2 (Figure 1) [34–37].
Tomato LeMFP1 associates with MARs of DNA to link
DNA to the NE and co-localizes with PCNA (proliferatingcell nuclear antigen), which suggests that it is involved in
DNA replication [38]. In addition, it binds to LeFPP, of which
over seven genes are present in the tomato genome as well as
homologues in other plant species including Arabidopsis [36].
Carrot NMCP1 [34] and its Arabidopsis homologues LINC1
and LINC2, on the other hand, are required for maintaining
overall nuclear structure as their deletion reduces the size of
nuclei and alters nuclear morphology [37].
Cytoskeletal associations with the NE
The plant NE not only associates with nucleoskeletal
structures but has also been shown to link to cytoskeletal
elements. However, a different organization of the cytoskeleton in plants and the lack of plant KASH domain sequence
homologues suggest different NE–cytoskeleton associations.
For instance, plants lack centrosomes and instead have
several MT nucleating sites: the NE surface, branching points
of pre-existing MT and the cortex underlying the plasma
membrane [39]. Central to animal, yeast and plant MT
nucleating sites, including MTOC and SPB, are γ -TuRCs
(γ -tubulin ring complexes) [1,39]. Homologues of yeast
γ -TuRC components have been identified in Arabidopsis
and two of them, AtGCP2 and AtGCP3, were shown to
have NE localization domains, essential for anchoring the
γ -TuRC to the plant ONM (Figure 1) [39]. While both
proteins are soluble, their NE localization domains are likely
to facilitate interactions with ONM-intrinsic proteins and
thereby anchor the γ -TuRC to the plant NE. However,
such ONM-intrinsic proteins have not been identified
so far.
The actin cytoskeleton is known to be associated with
the plant NE (Figure 1) and facilitates movement of the
nucleus [40]. Movement of the plant nucleus is essential in
various processes such as migration of nuclei into newly
forming root hairs and unequal cell division [40]. Movement
can occur in response to stimuli, for instance, mesophyll
cell nuclei move in response to blue light [41]. The links
between the actin cytoskeleton and plant NE remain to be
elucidated. Recently, a myosin tail domain, expressed as a
fluorescent protein fusion, was found to locate to the plant
NE, although how it is associated with the plant NE and its
functions remains unknown [42].
Targeting of proteins to the plant NE
The correct targeting of NE proteins, in particular INM
proteins, is essential for their proper function and for maintaining overall NE properties. Owing to the continuity of ER
(endoplasmic reticulum), ONM, pore membrane and INM,
it was thought that INM proteins simply diffuse through the
membranes [43]. Comprehensive studies in animal systems
have revealed that while passive diffusion may hold true
for membrane-bound proteins with nucleoplasmic domains
smaller than 25 kDa, it is slow, random and inefficient for
accumulating proteins in the INM. Instead, several previous
lines of evidence suggest that INM protein import is active,
regulated and, similar to soluble protein import, dependent
on NLS, karyopherins and the Ran cycle [44,45]. Targeting
of INM proteins is thought to start with sorting at the
translocon, where in insect cells importin α-16 associates
specifically with INM proteins, which are differentiated from
other membrane-intrinsic proteins by their transmembrane
domains [46–48]. This event demonstrates that rather than
random diffusion of INM proteins through the ER, INM
proteins are specifically recognized and are likely to be
directly targeted to the INM [45,46,48]. Many INM proteins
have been found to have classical NLS, which are recognized
by the import machinery and are partly essential for correct
targeting to the INM [44,45]. Import of INM proteins
was found to be energy dependent [49] and may require
changes in NPC structure, for example provided by flexible,
sliding nucleoporins [4,44,45]. In addition, FG nucleoporins
are required for INM protein translocation and some FG
nucleoporins, such as POM121, are associated with or are in
close proximity to the pore membrane [4,45].
Targeting of NE proteins in plants is far less well
understood. However, it can be hypothesized that it is similar
to that in animal and yeast systems. First, plants show similar
mechanisms for the import and export of soluble proteins
through NPC [8,32,50]. At least 17 importin-β and eight
importin-α homologues as well as three exportin homologues
have been identified in plants [1,32]. Most members of
the Ran cycle have been characterized [8] and putative
nucleoporins with FG repeats have been found in silico
([51]; and K. Graumann and D.E. Evans, unpublished work).
Secondly, some plant NE proteins such as DMI1, AtSUN1
and AtSUN2 and the WIPs contain putative classical NLS,
further indicating the possibility of active protein transport to
the plant INM [10,17,24]. Thirdly, our research group showed
that the N-terminus and first transmembrane domain of
human LBR fused to GFP (green fluorescent protein; LBR–
GFP) localize to the INM in tobacco cells, strongly suggesting
that mammalian INM targeting signals are correctly
recognized by the plant NE targeting machinery [52,53].
Apart from the seemingly conserved INM targeting
mechanisms, plants also have a specific NE targeting
mechanism for NE-associated proteins, which do not
exist in other kingdoms [32]. This system is based on
the WPP domain, which is present in LeMFP1, MAF1
(MFP1-associating factor 1) and its Arabidopsis homologues
WPP1 and WPP2 as well as Arabidopsis RanGAP [11,32].
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Whereas in animals RanGAP is anchored to the ONM by
SUMOylation (SUMO is small ubiquitin-related modifier)
and binding to RanBP2 (Ran-binding protein 2)/Nup385,
in plants the WPP domain is essential for association with
the ONM and NPC [32]. A membrane-anchored protein
complex consisting of at least one member of the WIPs and
WITs (Figure 1) recognizes the WPP domain and anchors
the proteins to the NE [11]. The WIPs and WITs in turn
are thought to retain their localization at the ONM and
pore membrane by interactions with NPC components
[11,32]. The RanGAP targeting is specific to undifferentiated
Arabidopsis root tip cells, suggesting that this process is linked
to development and is more complex than in animal cells [32].
Conclusions and future prospects
The work reviewed here reveals significant progress in
describing the protein constituents of the plant NE. With this
information, the field is rapidly expanding to allow description of fundamental mechanisms. These include the processes
of NE breakdown and reformation in mitosis, nucleocytoskeletal interactions, nuclear and chromatin anchorage
and the control of gene expression and the processes involved
in the formation, function and maintenance of nuclear pores.
Funding
We acknowledge support from the Leverhulme Trust [grant number
F/00382/H] and Oxford Brookes University.
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Received 30 September 2009
doi:10.1042/BST0380307
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