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State of the Field
The Cytoskeleton Becomes Multidisciplinary
Geoffrey O. Wasteneys* and Zhenbiao Yang*
Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4
(G.O.W.); and Center for Plant Cell Biology, Department of Botany and Plant Sciences,
University of California, Riverside, California 92521–0124 (Z.Y.)
It is now becoming clear that the plant cytoskeleton
is not just involved in fundamental processes like
mitosis, cytokinesis, cell polarity, and intracellular
trafficking. For many years, the cortical cytoskeleton’s
specialized function in plant cell wall construction
and morphogenesis has been investigated, but other
unique attributes of plants, such as the regulation of
water loss through stomatal guard cell movements,
pollen tube growth through female reproductive tissue, and elaborations like trichomes and root hairs,
also depend on the cytoskeleton. Today it is apparent
that the plant cytoskeleton plays an active role in
modulating the response of plants to changes in their
environment, including encounters with other organisms. It is therefore not surprising that the cytoskeleton
is no longer confined to the field of cell biology and
that research in a wide range of plant science disciplines, including macromolecular structure, development, hormone action, and environmental stress, will
all include important studies on the cytoskeleton. With
Plant Physiology’s coverage of this wide range of plant
science disciplines, a focus issue on the cytoskeleton is
timely. Our focus on the cytoskeleton issue begins with
four Update articles and includes nine research articles
spanning a wide range of disciplines.
It is well established that several hormones including
auxins, gibberellins, brassinosteroids, and ethylene
influence the organization of cortical actin microfilaments and/or microtubules, implicating a role for these
cytoskeletal arrays in hormonal responses. A paper in
the November issue of Plant Physiology from Mike
Bevan’s group (Li et al., 2004) shows that Arabidopsis
(Arabidopsis thaliana) mutants, in which a NAP-like
gene is knocked out, are affected in sugar responses,
implicating actin in the regulation of this process. NAP
(NCK-associated protein) is a subunit of the WASP
family verprolin homologous protein complex that
regulates the conserved actin nucleating Arp2/3 complex. The cytoskeleton has also been implicated in
abiotic stress responses such as in osmotic regulation
and is known to modulate the activity of ion channels.
Both plant-pathogen and symbiotic interactions involve changes in cell polarity and cellular trafficking
in plants and thus are intimately associated with the
* Corresponding authors; e-mail [email protected],
[email protected]; fax 604–822–6089, 951–827–4437.
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900130.
reorganization of the cytoskeleton. An Update article in
this issue by Daigo Takemoto and Adrienne Hardham
(Takemoto and Hardham, 2004) discusses cytoskeletal
responses and functions during encounters between
plants and other organisms.
Specific functions of the cytoskeleton depend on how
microtubules and microfilaments are distributed and
arranged, and how their behavior is modified by proteins that directly associate with both intact polymers
and their subunit monomers (Wasteneys and Galway,
2003; Sedbrook, 2004). Significant progress has been
made in the identification and functional analysis of
cytoskeleton-associated proteins involved in nucleation, membrane anchoring, dynamics (e.g., growing
and shrinking of polymers), severing, and polymer
cross-linking. In this issue, we highlight the most recent
work on the factors influencing microtubule and actin
microfilament behavior, and discuss the advantages
and limitations of live probes to investigate previously
undescribed cytoskeletal functions (Wasteneys and
Yang, 2004). Sherryl Bisgrove, Whitney Hable, and
Darryl Kropf (Bisgrove et al., 2004) update plus-end
tracking proteins, an emerging group of diverse microtubule-associated proteins that may hold the key to
understanding how microtubule polarity is put to work
in cells. And recent progress in understanding plant
motor proteins, including an astounding complement
of kinesins and myosins, is covered in an article by YuhRu Lee and Bo Liu (Lee and Liu, 2004).
Two research articles in this issue advance our
knowledge of how microtubule-associated proteins
(MAPs) work in plant cells. Van Damme et al. (2004;
see cover) demonstrate that green fluorescent protein
(GFP)-tagged MAP65-1 and MAP65-5 are localized to
different subpopulations of cortical microtubules in
tobacco BY-2 cells, whereas GFP-MAP65-4 is localized
to a specific array of microtubules that rearranged to
form spindles. Shoji et al. (2004) identify the SPIRAL2
protein and confirm that this 94-kD HEAT repeatcontaining protein interacts with cortical microtubules.
Two intriguing findings of this study are that the spr2
mutants have heightened sensitivity to microtubuledisrupting herbicides that target tubulin, and despite
the propensity for right-handed twisting in spr2 mutants, when combined with the lefty alpha tubulin point
mutations (Thitamadee et al., 2002), left-handed organ
twisting is accentuated. The long-recognized biotechnological significance of point mutations in tubulins for
effective herbicide use in agriculture is highlighted by
Plant Physiology, December 2004, Vol. 136, pp. 3853–3854, www.plantphysiol.org Ó 2004 American Society of Plant Biologists
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3853
Wasteneys and Yang
Délye and coworkers, who explore the molecular basis
for herbicide sensitivity and cross resistance (Délye
et al., 2004). It is now clear that microtubule dynamics
play an important role in tip-growing root hairs, and in
this issue, Van Bruaene et al. (2004) use a MAP4
microtubule binding site-GFP line to follow microtubule organization and behavior. They show for the first
time in Arabidopsis root hairs an extensive array of
endoplasmic microtubules, and highlight likely search
and capture behavior of microtubules in these tipgrowing protuberances of root epidermal cells.
On the actin side of the cytoskeleton, a report in this
issue by Fan et al. (2004) has identified a novel actinsevering protein from lily, LdABP41, which adds to the
growing list of actin-binding proteins mediating actin
dynamics and reorganization. The role of the actin
cytoskeleton in the modulation of intracellular signaling is highlighted in Wang et al.’s report in this issue
describing an inhibitory effect of actin microfilaments
on extracellular calcium influxes and cytosolic calcium
accumulation in Arabidopsis pollen (Wang et al., 2004).
Developing new ways of documenting the activity
and distribution of actin microfilaments remains challenging, and caution is still required in the use of fluorescent fusion proteins. Two articles in this issue focus
on the relative advantages and disadvantages of two
live probes for labeling actin microfilaments. Ketelaar
et al. (2004) demonstrate that GTP-mTalin can alter the
dynamic activity of microfilaments, generate defects in
cell development, and may not faithfully report all
microfilament arrays in plant cells. Similarly, Sheahan
et al. (2004) demonstrate how well a GFP construct
incorporating one of fimbrin’s actin-binding domains
works in several plant systems in comparison to available GFP-Talins.
Finally, identifying the functional connections between microtubule and actin microfilament arrays is an
area of tremendous importance. An intriguing glimpse
is provided in an article published in this issue in which
a kinesin with actin microfilament-binding activity and
association with cortical arrays in cellulose-rich cotton
fibers is identified (Preuss et al., 2004). In future issues
of Plant Physiology, we hope to see more studies that
consider the functional aspects of actin microfilaments
and microtubules as integrated networks in plant cells.
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Délye C, Menchari Y, Michel S, Darmency H (2004) Molecular bases for
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Fan X, Hou J, Chen X, Chaudhry F, Staiger CJ, Ren H (2004) Identification
and characterization of a Ca21-dependent actin filament-severing protein from lily pollen. Plant Physiol 136: 3979–3989
Ketelaar T, Anthony RG, Hussey PJ (2004) Green fluorescent proteinmTalin causes defects in actin organization and cell expansion in
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Lee Y-RJ, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one
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Li Y, Sorefan K, Hemmann G, Bevan MW (2004) Arabidopsis NAP and PIR
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Sedbrook JC (2004) MAPs in plant cells: delineating microtubule growth
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Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin
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Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima
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Plant Physiol. Vol. 136, 2004
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Copyright © 2004 American Society of Plant Biologists. All rights reserved.