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Update on 1TIPs and Microtubule Regulation
1TIPs and Microtubule Regulation. The Beginning of the
Plus End in Plants1
Sherryl R. Bisgrove*, Whitney E. Hable, and Darryl L. Kropf
Department of Biology, University of Utah, Salt Lake City, Utah 84112–0840 (S.R.B., D.L.K.); and Department
of Biology, University of Massachusetts Dartmouth, North Dartmouth, Massachusetts 02747–2300 (W.E.H.)
Plants have evolved novel microtubule (MT) arrays
to regulate cell division and cell expansion. How these
MT arrangements are managed has been a question
of long-standing interest to plant cell biologists. Do
plants have unique ways of regulating MTs or have
they co-opted mechanisms that are familiar to us from
studies in animal and fungal cells? This Update focuses
on the MT plus-end-tracking proteins (1TIPs), a relatively recent addition to the repertoire of MT regulatory proteins. Although the study of 1TIPs in plants is
just beginning, the emerging data indicate that some,
but not all, 1TIPs are conserved in the green lineage
and that plants have at least one family of 1TIPs that
is unique. Plants, it seems, organize their MT arrays
via a combination of novel and phylogenetically conserved mechanisms.
MT ARRAYS IN THE GREEN PLANT LINEAGE
Although the structure of an individual MT is highly
conserved in all eukaryotes, higher order MT arrays
vary widely, from spindles to flagella, and during
a single cell cycle MTs rearrange in a precise and
predictable sequence that is characteristic of the phylogenetic lineage. In many eukaryotic lineages, cells
contain centrosomes that serve as MT-organizing
centers. During interphase, MTs emanating from the
centrosome extend outward to the cell cortex, forming
radial structures that function in intracellular transport and cytoplasmic organization. In mitosis, MTs
reassemble into a spindle that mechanically segregates
chromosomes to daughter nuclei and participates in
division plane specification.
MT arrays are organized quite differently in plants
(Wasteneys, 2002). Higher plant cells lack centrosomes
and the associated radial array. Instead, interphase
MTs are found in the cortex of the cell, where they are
arranged parallel to one another and generally transverse to the direction of cell expansion. As cells near
mitosis, the cortical array rearranges into a narrow
band that encircles the nucleus and portends the
1
This work was supported by the National Science Foundation
(award nos. IBN 0110113 and IBN 0414089).
* Corresponding author; email [email protected]; fax
801–581–4668.
www.plantphysiol.org/cgi/doi/10.1104/pp.104.051037.
future division plane. This preprophase band (PPB)
is transient, disassembling as the spindle forms. At
telophase, yet another MT array, the phragmoplast, is
assembled between daughter nuclei. The phragmoplast is a cylindrical array composed of two opposing
sets of parallel MTs that transport Golgi vesicles to the
midzone, where they fuse to form the nascent cell
plate. With time, the phragmoplast and growing cell
plate expand outward to the cortex, where fusion
occurs at the site previously marked by the PPB. After
cytokinesis, cortical MTs reappear and become organized into parallel arrays. The cortical interphase
array, PPB, and phragmoplast are unique to the green
lineage, and there is much interest in understanding
their structure, function, and regulation. The observation that plant cells transiently form several clearly
discernable MT arrays during each cell cycle highlights the need to have mechanisms to rapidly assemble, organize, and disassemble MTs.
1TIPs AND MT ORGANIZATION
MT assembly and organization are regulated by the
inherent dynamics of the tubule and by an array of
regulatory proteins termed MAPs (MT-associated proteins). The inherent dynamics, or dynamic instability,
of MTs is governed by their ends, which exhibit rapid
transitions between growing and shrinking states
(Desai and Mitchison, 1997). The minus end is generally capped and stabilized by a complex of nucleating
proteins, and MT dynamics are therefore primarily
governed by the properties at the plus end, which
elongates and shortens as it explores the cytoplasm.
Plus ends of growing MTs contain GTP caps resulting
from the addition of tubulin dimers with bound GTP.
The GTP cap is thought to regulate dynamics in the
following way: MTs containing a GTP cap preferentially elongate, whereas hydrolysis of GTP to GDP by
the inherent GTPase activity of tubulin induces a conformational change that favors shortening. Sometimes
MTs exhibit dynamics at both ends. Recent in vivo
observations in plant cells indicate that treadmilling,
defined as the loss of tubulin dimers from the minus
end coupled with addition at the plus end, causes MT
migration along the cell cortex and contributes to
changes in array organization (Shaw et al., 2003).
MT dynamics are also regulated by MAPs. Many
MAPs bind to the sides of MTs and stabilize,
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Bisgrove et al.
destabilize, or bundle the tubules. In 1999, a new
family of MAPs that preferentially accumulate at the
plus ends of MTs was discovered by observing the
movements of CYTOPLASMIC LINKER PROTEIN
170 (CLIP-170)-green fluorescent protein (GFP) in
living mammalian cells. The fusion protein formed
a comet that tracked the plus ends of growing MTs
(Perez et al., 1999), and this property is now the
defining characteristic of a family of proteins called
1TIPs. The number of 1TIPs, many structurally unrelated, identified in fungi and metazoans is growing
rapidly, and intense investigation is elucidating their
functions in cellular physiology. 1TIP association
alters the dynamic parameters of the plus end, usually
resulting in longer, more dynamic MTs. Long, dynamic MTs are ideal for searching the cellular milieu,
and when the plus ends encounter appropriate receptors, they are captured and stabilized. 1TIPs mediate
MT capture at the kinetochore of chromosomes and at
localized cortical sites, including cell ends in fission
yeast (Schizosaccharomyces pombe), a cortical crescent in
Drosophila melanogaster neuroblasts, the bud in dividing budding yeast (Saccharomyces cerevisiae), and the
leading edge in migrating cells. This local MT capture
orients polarized growth, spindle position, division
plane specification, and directional migration. Thus,
1TIPs regulate both MT dynamics and the structure/
polarity of the MT array. Several excellent reviews
concerning 1TIPs in non-plant cells have recently
appeared (Hayles and Nurse, 2001; Schuyler and
Pellman, 2001a; Carvalho et al., 2003; Galjart and
Perez, 2003; Howard and Hyman, 2003; Martin
and Chang, 2003; Mimori-Kiyosue and Tsukita, 2003;
Morris, 2003; Xiang, 2003; Gundersen et al., 2004), and
the reader is directed to these for more detailed
discussions. The study of 1TIPs in plants is just beginning and, following a brief consideration of mechanisms of plus-end accumulation, this Update focuses
on identifying potential 1TIPs in the Arabidopsis
(Arabidopsis thaliana) genome and discusses initial
research results.
PATHWAYS OF PLUS-END ACCUMULATION
Although detailed mechanisms have not been
worked out, there are three general pathways by
which 1TIPs are thought to accumulate at plus ends:
treadmilling, hitchhiking, and motor-driven transport
(Fig. 1; Carvalho et al., 2003). Treadmilling and hitchhiking involve transient binding to the plus end,
whereas motor-driven transport translocates proteins
along the MT to the plus end (Galjart and Perez, 2003).
1TIPs that treadmill preferentially bind to the plus
end of a growing MT and are released a short time later
as the plus end grows past. Treadmilling 1TIPs do not
translocate through the cytoplasm with the plus end
but instead bind and release at the same point in space
(Perez et al., 1999). Thus, the comet that appears to surf
the plus end when GFP-tagged proteins are visualized
Figure 1. Proposed mechanisms for plus-end binding. Green circles at
the plus end of the MT denote a-tubulin bound to GTP. See text for
details.
in living cells is an illusion caused by the 1TIPs
hopping on and off the end as it rockets past. Several
factors can contribute to preferential end localization
of treadmilling 1TIPs, including copolymerization
with tubulin dimers, high-affinity binding to MT
ends, and selective release from the tubule walls
(Fig. 1A; Schuyler and Pellman, 2001a; Carvalho
et al., 2003). High-affinity binding to a MT plus end
is facilitated by its unique chemical and structural
properties (Tirnauer et al., 2002). Rather than a cylinder, the plus end of a growing MT is an open sheet (for
review, see Carvalho et al., 2003). The edges of the
sheet are brought together, and the cylinder zips up as
the MT grows. Treadmilling 1TIPs may bind preferentially to the curved sheet conformation or to sites on
the internal surface of the tubule exposed only at the
plus end. The GTP cap at the plus end may also
facilitate binding. Selective release behind the elongating tip may be due to lower affinity of the treadmilling
protein for the closed cylinder and/or chemical modification of the tubule (e.g. GTP hydrolysis) or the
1TIP (e.g. phosphorylation; Schroer, 2001).
Plus-end tracking can also be accomplished by
hitchhiking. Hitchhiking 1TIPs bind the MT plus
end indirectly through a treadmilling protein and,
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1TIPs and Microtubule Regulation
like treadmilling proteins, appear to surf the plus end
but are not transported through the cytoplasm with
the growing MT (Carvalho et al., 2003). Some hitchhiking proteins participate in MT capture by serving as
bridging proteins between MTs and receptor proteins
at a capture site (Gundersen et al., 2004). In budding
yeast, 1TIPs provide bridges between MT and actin
cytoskeletons at specific sites and at specific times
during the cell cycle (Heil-Chapdelaine et al., 1999).
In motor-driven transport, the 1TIP is cargo on
a kinesin that walks toward the plus end (Fig. 1C). This
mechanism of plus-end accumulation differs from
hitchhiking and treadmilling in several regards. First,
motors allow proteins loaded onto MTs to be translocated through the cytoplasm and unloaded at target
sites. Second, 1TIPs using motor-driven transport are
found along the MT length, whereas treadmilling/
hitchhiking proteins localize preferentially at plus
ends with little or no protein associated with MT walls.
Third, motors with their 1TIP cargos stay attached to
shrinking MTs (Galjart and Perez, 2003). By contrast,
treadmilling/hitchhiking proteins fall off depolymerizing MTs, resulting in loss of the characteristic plusend comet. As a MT shifts to the shrinking state, the
GTP cap is lost and protofilaments splay apart, which
may prevent 1TIP binding (Carvalho et al., 2003).
Recent evidence indicates that plus-end accumulation may be considerably more complicated. A 1TIP
may associate with plus ends using two or even all
three mechanisms, and different organisms may use
distinct pathways to localize the same 1TIP family
member (Carvalho et al., 2003; Lee et al., 2003; Xiang,
2003; Zhang et al., 2003). Furthermore, many of the
1TIPs interact with one another leading to speculation
that there may be rafts of interacting proteins surfing
on the plus end of MTs, where they regulate MT
dynamics and capture (Coquelle et al., 2002; Galjart
and Perez, 2003).
1TIPs IN PLANTS
What is the nature of the plus ends of plant MTs?
One might expect many of the proteins found in
fungal and metazoan cells to be conserved in plants;
kinetochore MTs, for instance, capture chromosomes
in all eukaryotic cells. On the other hand, the phragmoplast, PPB, and cortical array are unique to plant
cells, and their regulation may require plant-specific
1TIPs. An increase in MT dynamics has been measured during PPB formation (Dhonukshe and Gadella,
2003; Vos et al., 2004), and it has been proposed that
this increase in dynamics may facilitate MT search and
capture in the PPB (Vos et al., 2004). PPB formation is
therefore an excellent candidate for regulation by conserved, or novel, 1TIPs.
To date, data documenting plus-end tracking have
been published for two plant proteins, phylogenetically conserved EB1, (Chan et al., 2003; Mathur et al.,
2003) and SPIRAL1 (SPR1), a 1TIP with family members found only in plant sequence databases (Nakajima
et al., 2004; Sedbrook et al., 2004). In addition, preliminary data indicate that the kinesin ATK5 is also a
novel type of 1TIP (C. Ambrose and R. Cyr, personal communication). To assess the extent to which
1TIPs are conserved in plants, we performed BLAST
searches of the Arabidopsis protein database at the
National Center for Biotechnology Information
(NCBI; http://www.ncbi.nlm.nih.gov/) using sequences from 1TIPs and their binding partners in
fungi and metazoans. This analysis indicates that
some 1TIPs are conserved in plants (Table I), while
others appear to be absent.
END BINDING 1
END BINDING 1 (EB1) proteins were the first plant
molecules identified as 1TIPs (Chan et al., 2003;
Mathur et al., 2003). EB1 proteins play important roles
in diverse organisms, ranging from human to fungal
cells. By regulating MT dynamics and mediating
attachment of MT ends to subcellular sites, they are
instrumental in assembling and aligning the mitotic
spindle, guiding polarized cell growth, and facilitating chromosome capture by spindles (for review, see
Schuyler and Pellman, 2001a; Carvalho et al., 2003).
The Arabidopsis genome contains three EB1 genes,
designated AtEB1a, AtEB1b, and AtEB1c; each predicted protein contains conserved domains and shares
significant sequence similarity with EB1 proteins from
other organisms (Table I). All three AtEB1 proteins are
predicted to contain a conserved amino-terminal calponin homology domain required for MT binding as
well as a conserved coiled-coil domain (EB1 domain)
thought to mediate protein-protein interactions (Bu
and Su, 2003).
GFP fusions with two of the Arabidopsis proteins,
AtEB1a and AtEB1b, label the faster-growing ends of
MTs in a characteristic comet shape in living cells (Chan
et al., 2003; Mathur et al., 2003). However, both fusion
proteins also localize to additional sites. AtEB1a-GFP is
found at the slower-growing minus ends of cortical
MTs, where it appears to mark MT nucleation sites in
the cortical array (Chan et al., 2003; Wick, 2003). EB1
proteins are found at MT nucleation sites (e.g. spindle
poles and centrosomes) in several organisms (Berrueta
et al., 1998; Morrison et al., 1998; Tirnauer et al., 1999;
Rogers et al., 2002; Tirnauer et al., 2002; Straube et al.,
2003), but it is not yet clear whether they anchor minus
ends (Askham et al., 2002; Louie et al., 2004) or serve as
an EB1 reservoir for binding the plus ends of recently
nucleated MTs (Rehberg and Graf, 2002). Curiously, the
GFP:AtEB1b fusion has a subcellular localization pattern that is different from that of the AtEB1a:GFP
fusion. In addition to MTs, GFP:AtEB1b also labels
internal membranes, including endoplasmic reticulum
and membranes that surround chloroplasts, mitochondria, and nuclei (Mathur et al., 2003).
Both AtEB1 fusions also label along the lengths
of MTs, a pattern that has been reported in cells
overexpressing EB1 (Schwartz et al., 1997; Tirnauer
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Bisgrove et al.
Table I. 1TIPs and interacting proteins found in plants
Potential Arabidopsis families were identified either from published reports or from database searches at NCBI. For sequences identified by database
searches, designation as a putative 1TIP or interacting protein was based on the presence of conserved protein domain structures (as predicted from
the Conserved Domain Database [Marchler-Bauer et al., 2003]) as well as BLASTP scores and E-values. –, Not done.
Evidence
Protein Family
EB1
Sequence(s) Used
for Comparison
Sequence(s) Found
in Arabidopsis Genome
NP_036457
(human EB1)
NP_190353
(AtEB1a; At3g47960)
NP_201056
(AtEB1b; At5g62500)
NP_201528
(AtEB1c; At5g67270)
NP_193830 (At4g20980)
NP_199245 (At5g44320)
MOE1
NP_594625
(fission yeast
Moe1p)
MAP215/DIS1 AAG34914
(Xenopus
XMAP215)
FORMIN
(Diaphanous)
MYOSIN
CLASP
LIS1 (NUDF;
Pac1)
KINESIN
SPR1
NP_565811
(MOR1/GEM1;
At2g35630)
BLASTP
Score
E-Value
154
3 3 10236
180
5 3 10244
176
9 3 10243
320
312
Protein
Domain
Predictions
References
Calponin
homology
and EB1
Chan et al. (2003); Gardiner
and Marc (2003); Mathur
et al. (2003); Meagher and
Fechheimer (2003)
1 3 10285
2 3 10283
EIF-3_zeta
Gardiner and Marc (2003)
590
1 3 102166
TOG, tau,
and HEAT
repeats
Tournebize et al. (2000);
Whittington et al. (2001);
Meagher and Fechheimer
(2003); Gard et al. (2004)
Deeks et al. (2002)
–
21 sequences
–
–
FH1 and FH2
–
17 sequences
–
–
NP_849997 (At2g20190)
179
7 3 10243
Reddy and Day (2001a)
Motor,
coiled-coil
and putative
calmodulin
binding
Mast at
Gardiner and Marc (2003)
C terminus
NP_201533
NP_177513
NP_565749
NP_192428
NP_566534
NP_850598
NP_173290
NP_190534
NP_197779
NP_173960
NP_974110
NP_566166
NP_567685
NP_197064
124
119
109
–
–
–
–
–
–
–
8 3 10227
2 3 10225
2 3 10222
–
–
–
–
–
–
–
BAA94248
(Drosophila
orbit)
CAD55133
(D. discoideum
Lis1)
ATK5 MCAKs
Kip3p
At2g03680
(At5g67320)
(At1g73720)
(At2g32700)
(At4g05190)
(At3g16060)
(At3g16630)
(At1g18550)
(At3g49650)
(At5g23910)
(At1g26360)
(At1g69230)
(At3g02180)
(At4g234960)
(At5g15600)
et al., 1999; Mimori-Kiyosue et al., 2000; Lignon et al.,
2003). In the Arabidopsis studies, the AtEB1 sequences
were placed under the regulation of the cauliflower
mosaic virus 35S promoter, which is known to drive
high levels of gene expression (Sanders et al., 1987), and
it is therefore possible that the observed localization
patterns do not accurately reflect endogenous AtEB1.
Unpublished data supports this concern; when AtEB1b:
GFP expression is driven by either the Hsp18.2 heat
shock promoter or 1.5 kb of AtEB1b upstream sequences, labeling is restricted to comet-shaped structures at fast-growing MT ends (R. Dixit and R. Cyr,
personal communication). These constructs label growing, but not shrinking, MTs consistent with the treadmilling mechanism of end accumulation found for
LisH and
WD-40
repeats
–
Reddy and Day (2001b)
Nakajima et al. (2004);
Conserved
Sedbrook et al. (2004)
sequences
in aminoand carboxyterminal
regions
non-plant EB1s. Furthermore, we have analyzed
AtEB1 localization using a polyclonal antibody directed against AtEB1c, and have observed labeling
only at MT ends in the cortical MT array (S.R. Bisgrove,
unpublished data). Further imaging studies are needed
to clarify AtEB1 localization patterns, and mutant
analyses are needed to address the functions of plant
EB1 proteins in regulating MT dynamics and mediating
MT search and capture.
EB1-Associated Proteins
The Arabidopsis database contains two sequences
that may represent EB1-binding partners of the Moe1p
(MTs overextended) family (Table I). In fission yeast,
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1TIPs and Microtubule Regulation
Moe1p binds the EB1 family member Mal3p, and
genetic and physical interaction studies indicate that
Mal3p and Moe1p may act as a complex that regulates
MT dynamics (Chen et al., 2000). Moe1p can itself
influence MT dynamics; as the name suggests, MTs in
moe1 mutants are unusually long (Chen et al., 2000).
Recent evidence indicates that a putative AtMOE1
interacts with AtEB1 in yeast two-hybrid assays
(R. Dixit and R. Cyr, personal communication), but
how it might regulate MTs in plant cells is unknown.
MAP215/DIS1 is a phylogenetically conserved family of proteins that includes XMAP215 in frogs, DIS1
in fission yeast, TOG in mammals, and MOR1/GEM1
in plants. These proteins regulate MT dynamics (for
review, see Hussey et al., 2002; Gard et al., 2004),
and emerging data suggest that they interact with
EB1. Dictyostelium discoideum EB1 colocalizes with
DdCP224 (the MAP215/DIS1 family member), and
the two proteins can be coimmunoprecipitated from
cytosolic extracts (Rehberg and Graf, 2002). Furthermore, Bim1p (budding yeast EB1) interacts with Stu2p
(the MAP215/DIS1 family member) in yeast twohybrid screens (Chen et al., 1998). In the Arabidopsis
genome, the MICROTUBULE ORGANIZATION 1
(MOR1) gene codes for a MAP215/DIS1 family member (Table I; Tournebize et al., 2000; Whittington et al.,
2001). The MOR1 protein colocalizes with MTs in the
preprophase band, spindle, phragmoplast, and cortical arrays (Twell et al., 2002), and mutant analyses
suggest that MOR1 does regulate MTs in the cortical
and cytokinetic arrays. Temperature-sensitive mutations in the amino-terminal region of the MOR1 protein cause disruption of cortical MTs in plants grown at
the restrictive temperature (Whittington et al., 2001),
and truncations that are predicted, but not yet proven,
to remove carboxy-terminal regions of the protein
disrupt cytokinesis during pollen development and
are sporophytically lethal (Twell et al., 2002). The
possibility that MOR1 and EB1 interact with each
other in plant cells is currently under investigation.
Additional proteins known to interact with EB1
include the adenomatous polyposis coli (APC) protein
from humans and Kar9p from budding yeast (Su et al.,
1995; Korinek et al., 2000; Lee et al., 2000; Miller et al.,
2000; Mimori-Kiyosue et al., 2000). Although these
proteins appear to be unrelated to each other at the
amino acid level, it has been proposed that they are
functionally equivalent since both proteins link EB1 at
MT plus ends to the cell cortex (Bienz, 2001; Nakamura
et al., 2001). Our searches of the Arabidopsis database
do not identify any proteins that might be related to
either APC or Kar9p based on sequence similarities.
The TANGLED1 (TAN1) protein of maize (Zea mays)
can bind MTs, and sequence comparisons suggest that
it may be distantly related to vertebrate APC (Smith
et al., 2001), but functional data linking TAN1 and EB1
are lacking. Biochemical and/or yeast two-hybrid
assays for proteins that interact with AtEB1 are needed
to identify plant proteins that might be functionally
related to APC or Kar9p.
Formins are a family of conserved proteins thought
to provide a link between MTs and actin, perhaps via
EB1. At the cell cortex, formins nucleate actin filaments
and regulate the rate of polymerization by capping the
fast-growing barbed ends (Evangelista et al., 2003).
Formins also participate in MT processes, although
their role is less clear. In mammalian cells, the formin
mDia stabilizes MTs (Palazzo et al., 2001) and may
interact with EB1 and APC (Gundersen et al., 2004).
During spindle alignment in budding yeast, actin
filaments nucleated by the formin Bni1p are thought
to provide tracks for the transport of MTs bearing
Bim1p and Kar9p at their plus ends to the cortex by
a myosin motor, Myo2p (Beach et al., 1999; Yin et al.,
2000). The Arabidopsis genome contains 21 putative
formin sequences and 17 myosin sequences (Table I;
Castrillon and Wasserman, 1994; Banno and Chua,
2000; Cvrckova, 2000; Deeks et al., 2002; Reddy and
Day, 2001a). (See Preuss et al. [2004; this issue] for
a discussion of plant myosins.) Since EB1, myosins, and
formins are all present in the Arabidopsis genome, it is
plausible that plants have a conserved pathway for
delivering MT ends to cortical receptors (see Fig. 2
below).
CLIPs
As the first protein shown to track the plus ends
of MTs, CLIP-170 is the prototype 1TIP (Perez et al.,
1999). CLIP family members have now been identified
in diverse phyla where they regulate MT dynamics
and appear to link MTs to intracellular sites (Pierre
et al., 1992; Dujardin et al., 1998; Brunner and Nurse,
2000; Lin et al., 2001). Although the overall sequence
similarity is not high among CLIPs, the proteins all
share conserved domains. The MT-binding region,
located at the amino terminus, consists of one or
more CAP-Gly domains; it is followed by a central
Figure 2. Hypothetical model for delivery of a plant MT to a cellular
receptor at a specific site (e.g. PPB, phragmoplast, root hair tip) along
actin filaments, based on models from yeast and fibroblasts (Gundersen
et al., 2004). EB1 binds a bridging protein associated with myosin,
which translocates toward the barbed (plus) end of the actin filament.
Genome analysis identifies EB1, myosins, and formins in Arabidopsis.
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Bisgrove et al.
coiled-coil and one or more putative metal-binding
motifs at the carboxy terminus (Brunner and Nurse,
2000; Goodson et al., 2003). BLAST searches, using
D. melanogaster CLIP-190 and the Arabidopsis protein
database at NCBI, identify several proteins with
E-values #9 3 10215. However, none of these proteins
appear to be bona fide CLIPs since they all lack the
conserved CAP-Gly MT-binding domain. Curiously,
plants may well lack CLIPs. However, when mammalian CLIP-170 is expressed in plant cells, it tracks MT
plus ends, indicating that the pathway that regulates
the binding of CLIP-170 to MTs is conserved in plants
(Dhonukshe and Gadella, 2003).
CLIP-Associated Proteins
CLIP-associated proteins, or CLASPs, bind both
CLIPs and MTs; they colocalize with CLIPs at MT
plus ends, where they have a stabilizing effect (Akhmanova et al., 2001). CLASPs link spindle MTs to
kinetochores and also promote polarized growth at the
leading edge of migrating fibroblasts (Akhmanova
et al., 2001; Maiato et al., 2003). BLASTsearches identify
a single Arabidopsis protein (Table I; Gardiner and
Marc, 2003) that is related to MAST/ORBIT, the
D. melanogaster CLASP family member. Although it is
unknown whether this putative AtCLASP is in fact
a 1TIP, its presence is intriguing since there are no clear
CLIP family members in the Arabidopsis genome.
In animals and yeast, CLIP-170 may function
through interacting with the dynactin complex and
cytoplasmic dynein. Dynactin is a multisubunit complex that activates the minus-end-directed MT motor,
cytoplasmic dynein, also a protein complex. Dynactin
also binds to MT plus ends, and mutational and
overexpression studies suggest that it is targeted to
plus ends via p150Glued and CLIP-170 (Goodson et al.,
2003). In Arabidopsis, obvious cytoplasmic dynein
and dynactin components are absent (Lawrence et al.,
2001).
LISSENCEPHALY 1
Humans carrying mutations in the LISSENCEPHALY
1 (LIS1) gene have a severe developmental brain deformity known as lissencephaly (‘‘smooth brain’’) type
1 that is thought to reflect a defect in neuronal migration
(Reiner, 2000). LIS1 proteins are conserved across large
evolutionary distances and have been shown to form
comet-like structures at the dynamic plus ends of both
growing and shrinking MTs (Han et al., 2001; Coquelle
et al., 2002; Lee, et al., 2003). They mediate dynein
activity and regulate MT dynamics by mechanisms that
are not well understood (Xiang et al., 1995; Lei and
Warrior, 2000; Liu, et al., 2000; Dawe et al., 2001; Han
et al., 2001; Tai et al., 2002; Lee et al., 2003). LIS1 family
members contain an N-terminal coiled-coil LisH domain that is important for dimerization (Cahana et al.,
2001), followed by several WD repeats that mediate
protein-protein interactions (Reiner, 2000).
The Arabidopsis database contains several predicted proteins with the same domain structures as
LIS1 family members, and three of them score well
when compared with D. discoideum LIS1 sequences
(Table I). Fourteen additional Arabidopsis genes are
predicted to encode proteins with a LisH domain but
no WD repeats. One of these, At3g55000, is the
TONNEAU1b (TON1) gene. Curiously, ton1 mutants
have disorganized cortical MTs and cannot make PPBs
(Traas et al., 1995). Whether this reflects a role for plant
LIS1 proteins in MT regulation or is simply a coincidence awaits experimental evidence linking putative
LisH proteins with MT regulation in plants.
LIS1 has been linked genetically and biochemically
with dynein/dynactin and CLIP-170 (Willins et al.,
1997; Coquelle et al., 2002; Tai et al., 2002; Lee et al.,
2003). As discussed above, there are no clear CLIP-170,
dynein, or dynactin proteins in the genome, so if
plants do have bona fide LIS1 family members, they
may function differently than they do in other eukaryotic cells.
Kinesins
The Arabidopsis genome has 61 kinesins (Reddy
and Day, 2001b; see article by Liu in this issue), and
recently one has been found that represents a unique
class of 1TIPs. ATK5 accumulates preferentially at MT
plus ends; however, in contrast with kinesins that rely
on motor activity to bring them to the plus ends of
MTs, ATK5 is a minus-end-directed kinesin that binds
to MT plus ends via the tail-stalk region of the protein
(C. Ambrose and R. Cyr, personal communication;
Preuss et al., 2004). ATK5 localizes to spindle midzones and phragmoplast leading edges, where MTs
are organized in interdigitating, anti-parallel arrays.
Phylogenetic analyses (Reddy and Day, 2001b) suggest
that the motor domains of several Arabidopsis kinesins are related to motors with known MT plus-end
activities in other organisms (Table I). Two sequences
are related to the mitotic centromere-associated kinesins (MCAKs) that bind to the ends of MTs and induce
depolymerization (Walczak et al., 1996; Maney et al.,
1998; Desai et al., 1999; Hunter et al., 2003), and three
sequences are related to Kip3p, a motor that positions
the spindle by linking MT plus ends to the cell cortex
in budding yeast (Schuyler and Pellman, 2001b). Many
other Arabidopsis kinesins await functional characterization, and any of those with MT plus-end-directed
motor activity could prove to be 1TIPs.
SPR1 Proteins
SPR1 is the only plant protein thus far identified as
a 1TIP serendipitously rather than by genome analysis. SPR1 was identified because roots and hypocotyls
of mutant plants have a right-handed helical twist that
is thought to result from abnormal cell expansion.
Cortical MT orientation is also abnormal in spr1; instead of a transverse orientation, cortical MTs form
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1TIPs and Microtubule Regulation
helical arrays with a left-handed pitch (Furutani et al.,
2000). SPR1:GFP fusions localize to MTs in the cortical
array, PPB, phragmoplast, and spindle (Nakajima et al.,
2004; Sedbrook et al., 2004). In the cortical array,
SPR1:GFP forms comet-like shapes on the ends of
growing, but not shrinking, MTs, indicating that it is
a 1TIP (Sedbrook et al., 2004). However, the binding of
SPR1 to MTs might be indirect since polymerized
tubulin failed to pull down detectable amounts of
a GST:SPR1 fusion protein in vitro (Sedbrook et al.,
2004), consistent with plus-end accumulation by hitchhiking. How SPR1 affects MTs and how these effects,
in turn, regulate cell expansion is unknown.
The SPR1 gene appears to encode a plant-specific
1TIP. The predicted protein is a small (12-kD), novel
polypeptide that belongs to a plant-specific family of
proteins. The Arabidopsis genome contains five other
SPR1-like genes that share high sequence identity
in their amino- and carboxy-terminal regions and
have variable sequences in the intervening regions
(Nakajima et al., 2004; Sedbrook et al., 2004), but their
association with MTs has not yet been reported. It is
plausible that plants have evolved a novel family of
1TIPs to regulate their unique MT arrays.
CONCLUSIONS AND FUTURE PERSPECTIVES
The study of 1TIPs in plants has an exciting
beginning. Initial GFP fusion analyses confirm their
presence on the plus ends of dynamic MTs, and
genome gazing suggests that several more putative
1TIPs await investigation. Interestingly, it appears
that some complexes of 1TIPs and their interacting
proteins identified in protists and metazoans are also
present in plants, while others are absent. Genes
coding for the CLIP/dynein/dynactin complex are
lacking in Arabidopsis, whereas a yeast pathway
using EB1 and actin to deliver MT ends to cortical
sites may be conserved (Fig. 2). Analyses of SPR1 and
ATK5 demonstrate that plants also have novel 1TIPs,
perhaps to organize unique plant MT arrays.
Undoubtedly, the next few years will provide explosive progress in this field. Putative 1TIPs will be
confirmed or rejected by analysis of GFP fusions in
vivo, and biochemical studies will identify interacting
proteins as well as novel 1TIPs. Analyses of mutants
and overexpressing lines will help unravel the function of these proteins in regulating MT dynamics and
MT search and capture in plant cells. We are beginning
to take large strides toward understanding how plants
organize their MTs.
ACKNOWLEDGMENTS
We thank Nick Peters for critically reading the manuscript and David
Gard for drawing the MTs shown in Figure 1.
Received August 6, 2004; returned for revision September 30, 2004; accepted
October 12, 2004.
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