Download Signaling tip growth in plants Zhenbiao Yang

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Signaling tip growth in plants
Zhenbiao Yang
Tip growth is an extreme form of polar growth modulated by
both intrinsic and extrinsic spatial cues. Pollen tubes and root
hairs have been used as model systems to investigate tip
growth signaling in higher plants. Recent studies have focused
on tip-localized Ca2+ gradients and Rho GTPases in pollen
tubes and a series of mutants affecting root hair tip growth.
These molecular and genetic markers will serve as stepping
stones towards uncovering tip growth pathways in plants.
Addresses
Plant Biotechnology Center, The Ohio State University, 1060 Carmack
Road, Columbus, OH 43210, USA; e-mail: [email protected]
Current Opinion in Plant Biology 1998, 1:525–530
http://biomednet.com/elecref/1369526600100525
© Current Biology Ltd ISSN 1369-5266
Introduction
Cell polarity, characterized by asymmetric distribution of
subcellular structures and molecules, is a fundamental
attribute to the development of all eukaryotic organisms.
The unique significance of cell polarity in plant development is underscored by the fact that, in plants, cell
morphogenesis is largely defined by spatially organized
cell walls. Moreover, the position of sessile cells rather than
their lineage has a predominant role in dictating their
developmental fates. Because it is difficult to study the
control of cell polarity in tissues or organs composed of
multiple interacting cell types, most studies on plant cell
polarity have been focused on readily accessible tip-growing cells such as fucoid zygotes, root hairs, and pollen
tubes. These cells exhibit many crucial aspects of cell
polarity development.
maintaining this cytoplasmic polarity [7]. Obviously the
regulation of actin and microtubule dynamics needs to be
coupled to the tip growth signaling events in order to modulate growth direction and rate.
Major questions about tip growth are: first, what are the
signaling pathways that control the selection and establishment of the cortical site for tip growth? Second, what is the
machinery involved in polar secretion and how is it linked
to the signaling pathways? Finally, how are the pathways
coupled to the cytoskeleton to regulate vesicle transport
and cytoplasmic polarity? Similar questions regarding
polarized growth such as the formation of buds and mating
tubes (‘shmoos’) in Saccharomyces cerevisiae have been
investigated extensively [1,8]. In yeast, a signaling network involving several small GTPases controls polarity
establishment, cytoskeletal organization, polar secretion,
and cell wall assembly. The heart of this network is
CDC42, which is a Rho family small GTPase that regulates actin polarization upon activation by various spatial
cues [1]. In addition, a CDC42-independent Sec3p pathway is required for polarized growth in yeast [9]. Sec3p
shows polar localization to the site of growth and recruits to
exocysts (containing complexes of proteins critical for polar
secretion) to the same site. Are there similar pathways
involved in the regulation of tip growth in plants or are
there unique tip growth pathways in plants?
This review focuses on recent advances in addressing
these questions in the pollen tube and root hair systems.
For tip growth in Fucus zygotes, the reader is referred to
recent reviews [2••,10].
Recognition and interpretation of spatial cues
Intrinsic and extrinsic tip growth cues
Tip growth is dependent upon polarized exocytosis of
Golgi vesicles to a single defined site of the cell. On the
basis of what is known about tip growth in plant cells and
cell polarity development in yeast and mammals [1,2••,3•],
a general model for tip growth pathways is proposed
(Figures 1 and 2). Tip growth begins with the selection and
establishment of a cortical site of the cell at which vesicles
will dock and fuse [2••]. These processes require a signaling network to recognize and interpret intrinsic and
extrinsic spatial cues that determine the site and the direction of tip growth. The signaling network must orchestrate
the secretory machinery in such a way that Golgi vesicles
dock and fuse only at the specified site. To maintain tip
growth, vesicles have to be actively targeted to the tip via
the actin cytoskeleton [4]. Consequently, tip-growing
cells are organized such that they are composed of the
vesicle-rich apex, the subapical region containing various
organelles and the nucleus, and the vacuole-occupied
basal region [5,6]. Microtubules appear to be involved in
Both internal and external cues are known to determine
the site of tip growth initiation and the direction of tip
growth. In the absence of external cues, Arabidopsis pollen
tends to germinate near one end of the pollen grain
(R Heath and Z Yang, unpublished data), and root hairs
emerge from the apical end of epidermal cells and invariably grow away from the root axis [11,12•]. The nature of
these internal cues and their mode of action are unknown.
Pollen presents the best example of externally controlled
tip growth. When pollen grains land on the stigma, a
pollen tube will emerge from the aperture closest to papillar cells, suggesting the presence of a stigma-derived
signal [13•]. To deliver sperm to the egg, pollen tubes
must penetrate the stigma, travel through the transmitting
track, and enter the ovule. Cues for guidance within the
stigma and the transmitting track are most likely to
involve extracellular matrix components such as glycoproteins and lipids [14,15], and then targeting of tubes to
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Cell biology
Figure 1
Spatial Cues
Internal cues
External cues
Signal recognition
Recruitment and activation
of signaling apparatus
(e.g.,Rop1 GTPase, Ca2+)
Establishment of
tip growth sites
Actin
filaments
Secretory machinery
Polarity
maintenance
Feedback
regulation
Microtubules
Vesicle accumulation
in the apex
Localized secretion
Cytoplasmic
polarization
Plasma membrane growth
and cell wall assembly
Tip growth
Current Opinion in Plant Biology
A working model for tip growth pathways. The model describes the
generalization of current understanding of tip growth in pollen tube,
root hair and Fucus zygote systems. It should be noted that detailed
mechanisms for polarized growth are most likely to differ among
various systems. Substantial evidence is available for the participation
of Rop1 and Ca2+ in the establishment of tip growth sites and for the
involvement of the actin and microtubule cytoskeleton in tip growth.
Many events or components in the pathways remain to be identified,
however, and the actual signaling pathways are likely to be complex.
ovules requires chemoattractants derived from the female
gametophyte [16]. Repulsive cues are also expected to be
involved in guidance as only one tube grows towards each
ovule [13•].
Establishment of tip growth sites
For in vitro germinated pollen, the direction of tube
growth is manipulated by electrical currents, sugar and
Ca2+ gradients, but roles of these external cues in vivo
guidance remain unclear [17]. Nonetheless, pollen tube
guidance seems to share striking similarities with animal
axon guidance that requires adhesive, attractive, repulsive
and electric cues [18,13•]. How the guidance cues are recognized by pollen is unknown, but, in Arabidopsis, POP2
and POP3 genes are good candidates for this role [18];
pollen tubes from the pop2 and pop3 double mutant grow
normally within the transmitting tract but are unable to
find their way to the ovule, suggesting their specific role in
the signaling of ovule-derived factors [18]. Pollen-specific
receptor-like kinases (PRKs) from tomato have been localized to the plasma membrane of pollen tubes and might
play a role in pollen recognition [19].
In yeast, various spatial cues recruit and activate a unifying
signaling apparatus which controls the establishment of a
polar site [1,8]. Evidence is emerging that a unifying signaling mechanism also controls the establishment of tip
growth sites. Ca2+ is one of the best studied molecules
involved in this mechanism.
Localized accumulation of Ca 2+ at the cortical site for
tip growth has been demonstrated in various systems
including pollen tubes, root hairs, Fucus zygotes and
fungal hyphae [20–23]. For instance, pollen tubes contain a tip-focused intracellular Ca 2+ gradient ranging
from 10 µM at the tip to < 0.2 µM at the base [22,24 •].
Several recent studies suggest a critical role for the gradient in the control of tip growth [22,25–27,24•].
Experiments involving localized release of caged Ca 2+
or Ca2+ chelators in the apex of pollen tubes and root
hairs indicate that asymmetric distribution of intracellular Ca2+ alone is sufficient to establish the site of tip
growth [26,12 •].
Signaling tip growth in plants Yang
527
Figure 2
(a)
MT
GV
. .. . . . . . . .. .
V
. .. . . . . . . .. .
ER
M
MF
Rop1
Ca 2+ channel
M: mitochondria
ER: endoplasmic reticulum
MT: microtubules
GV: Golgi vesicles
Ca 2+
MF: actin microfilaments
V: vacuoles
(b)
Current Opinion in Plant Biology
Molecular and structural polarity in tip growing cells. (a) Major structures and molecules known to be critical for tip growth in pollen tubes or root
hairs. (b) Immunolocalization of Rop1Ps in pea pollen tubes (reproduced with permission from [30]).
Tip-localized plasma membrane Ca2+ channel activities
are at least partially responsible for the generation of the
tip-focused Ca2+ gradient [25–27,12•]. Although Ca2+
channels appear to be localized throughout the apical
dome of pollen tubes, only those localized to the extreme
apex are the most active [26,27]. Putative plasma membrane Ca2+ channels have also been polarly localized to the
tip of Fucus zygotes [28]. Intracellular release, however,
may also be involved in the generation of the Ca2+ gradient [29••]. Molecular identification of Ca2+ channels in
plants will be a critical step in elucidating the mechanism
behind the formation of the Ca2+ gradients. Uncovering
other signaling events involved in the establishment of tip
growth sites should also provide clues to this mechanism.
An exciting recent discovery in tip growth signaling came
from studies on tip-localized Rop GTPases [30,31••]. Rop is
a plant-specific GTPase of the Rho family that includes
CDC42, Rac, and Rho from fungi and animals [32,33•]. The
Rho-family GTPases are key regulators of actin cytoskeletal
organization and many other cellular processes in fungi and
animals [34]. Rop evolved prior to the divergence of Rac and
CDC42 and might have functions similar to those of CDC42
and Rac [33•]. A portion of Rop1, a pollen-specific isoform,
appears to be localized to the apical plasma membrane with
a tip high gradient, implying a recruitment of Rop1 to the
growth site [30]. This localization is particularly interesting,
because it is analogous to that of yeast CDC42 at the bud
emergence and growth sites [35].
When expressed as a GFP fusion protein in fission yeast,
Rop1 is also localized to the site of growth [33 •].
Overexpression of Rop1 in fission yeast caused non-polarized growth [33•], which is also induced by constitutively
active cdc42 mutants. Microinjected anti-Rop antibodies
specifically inhibit pollen tube growth [31••]. Interestingly,
this effect is more similar to loss-of-function cdc42 mutations in fission yeast (growth arrest) than in budding yeast
(enlarged cells unable to bud) [8]. Preliminary results show
that overexpression of Rop1 transformed normal cylindrical
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Cell biology
tubes into bulbous tubes (H Li and Z Yang, unpublished
data). These results indicate that Rop controls not only the
establishment of cell polarity but also tip growth, as does
CDC42 in tip-growing fission yeast [8].
The bulbous phenotype is analogous to tip swelling accompanied by non-localized intracellular Ca2+ accumulation
when arrested pollen tubes resume growth [22,26]. Further,
anti-Rop antibody-induced growth inhibition is potentiated
by a lower threshold of extracellular Ca2+ concentration and
a subinhibitory concentration of caffeine [31••]. Although the
mechanism behind the Rop–Ca2+ interaction is unknown, an
attractive explanation for these data is that Rop regulates
localized accumulation of intracellular Ca2+, which is thought
to be involved in the regulation of exocytosis through annexins [27,36]. The Rho-family GTPases also regulate
intracellular Ca2+ release and plasma membrane Ca2+ channels in animal cells [37,38]. Thus, Rop could modulate the
Ca2+ gradient by integrating various tip growth spatial cues.
In this regard, Rop may be analogous to the yeast CDC42,
which integrates bud site selection, pheromone, and pseudohyphal growth signaling pathways to control polarity
establishment through actin polarization [1].
Whether Rop regulates actin organization in pollen tubes
remains to be determined. Nonetheless, this role would be
difficult to compromise with recent findings that suggest
pollen tubes do not contain apical actin networks [39]. Tipassociated actin filaments have been demonstrated in
fucoid zygotes and play a crucial role in the establishment
of polarity [2••,40]. A Rac-like GTPase has been identified
in Fucus and has also been localized to the tip, providing a
good candidate for regulating polarity establishment
through organizing the tip-associated actin or other tip
plasma membrane-associated asymmetries (J Fowler and
R Quatrano, personal communication).
In summary, current evidence suggests that a Rop
GTPase controls the establishment of tip growth sites,
analogous to CDC42 in the control of polarity establishment in yeasts. The mechanism of Rop-dependent
polarity control, however, seems to be unique in that it
might regulate the tip-focused Ca2+ gradient, which has
yet to be shown in yeasts.
Cytoskeletal regulation of tip growth
Recent identification of several cytoskeleton-associated
proteins [4] may provide a starting point for understanding
how cytoskeletal dynamics is regulated by the signaling
network that controls tip growth.
Multiple isoforms of the actin-binding protein profilin are
found in pollen [41]. Profilins have been implicated in the
regulation of actin dynamics in Tradescantia stamen hair
cells and thus may also have a similar role in pollen tubes
[41]. In addition, pollen profilins may also participate in
signaling, as suggested by their ability to alter the phosphorylation of specific pollen proteins [42]. Unfortunately,
the uniform cytoplasmic localization of profilins in pollen
tubes revealed by immunolocalization and in live cells was
not informative regarding their roles in pollen [43].
Maize pollen profilin isoforms show differential capacities
to interact with proline-rich motifs, which are correlated
with their activities in altering actin dynamics in plant cells
[44••]. In animals and yeast, profilin interacts with prolinerich formin-homology domain proteins, apparent
downstream targets of Rho GTPases in the regulation of
actin dynamics [45]. Interestingly, a Rho-like GTPase may
also regulate actin organization in pollen tubes [31••].
Another potential regulator of the actin cytoskeleton is calcium-dependent protein kinases that associate with
microfilaments and are implicated in pollen germination
[46,47]. More attention needs to be given to the involvement of these actin-associated proteins in the regulation of
the actin cytoskeleton in tip-growing cells.
Tip growth mutants
Although biochemical and molecular studies described
above have shed some light on tip growth mechanisms, these
studies must be complemented with genetic approaches to
fully elucidate tip growth pathways, as in the study of yeast
cell polarity control. Indeed, some new insights into tip
growth in plants have been obtained by mutant analyses.
Root hairs serve as a model system for genetic analyses of
tip growth because they are dispensable and easy for
mutant screen [48,49]. Three loci affecting maize root hair
elongation and morphology were identified [49]. Mutations
in RTH1 are defective in hair elongation. RTH1 encodes a
protein with similarity to Sec3p (P Schnable, personal communication), raising the possibility that the Sec3p pathway
and exocyst might also be involved in tip growth in plants.
Exocyst is also critical for polarized secretion in mammalian
epithelial cells [50].
Seven complementation groups of tip growth mutants from
Arabidopsis have been reported and are divided into three
classes according to their phenotypes and genetic interactions [11,48,51,52] (see Figure 3). The hair initiation
mutants (rhd6) show reduced hair numbers and altered initiation sites and are rescued by auxin or ethylene,
suggesting a role for RHD6 in controlling the site of root
hair initiation [11]. Growth site establishment mutants
exhibit abnormal growth site morphology (rhd1) or fail to
undergo tip growth (rhd2).
Tip growth maintenance mutants (rhd3, cow1, tip1 and rhd4)
display various morphological changes. Consistent with
pleiotropic effects of some of these mutations in cell types
other than root hairs [52,53], this class of genes is most likely to be involved in polar secretion, cytoskeletal
organization, cell wall assembly, and cell expansion. RHD3
affects vacuole enlargement and Golgi vesicle accumulation
at the tip [53]. Recently, RHD3 has been shown to encode a
novel GTP-binding protein, suggesting its potential role in
Signaling tip growth in plants Yang
tubes, and root hairs. The review focuses on the development of cortical sites
that control polar growth and asymmetric cell division in Fucus zygotes.
Evidence is presented that the cortical site involves localized cytosolic Ca2+,
plasma membrane Ca2+ channels, and the actin cytoskeleton, which are all
required for the establishment of cell polarity and for polar secretion.
Figure 3
Selection Establishment Maintenance/growth
COW1
RHD6
RHD2
RHD1
RHD4
RHD3
TIP1
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Tip growth
Current Opinion in Plant Biology
A genetic pathway for root hair tip growth in Arabidopsis. The pathway
was proposed on the basis of phenotypic analyses of single and
double mutants (see [11,48,51]). The mutants described are classified
into three groups according to the proposed tip growth pathways
described in Figure 1. The initiation mutants show changes in the
number of root hairs and the position of hair initiation. Affected genes
are predicted to participate in early signaling of root hair initiation cues.
The establishment mutants show loss of polarity in the root hair proper.
These genes are expected to be required for the interpretation of tip
growth cues. The maintenance/growth mutants affect root hair
morphology and elongation. This class of genes are most likely
involved in cytoskeletal organization, secretion, and cell wall asembly.
signaling these processes [54••]. Genetic analyses of tip
growth in root hairs, therefore, will not only reveal tip
growth mechanisms but also shed light on other fundamental cellular processes.
Conclusions
Significant progress has been made towards understanding signaling pathways leading to tip growth in plants.
The tip-focused Ca2+ gradient is a unifying mechanism for
the establishment of tip growth sites in many tip growth
systems, and a Rop GTPase is emerging as another key
player in regulating this process in pollen tubes, probably
by interacting with the Ca2+ signaling. Future work
should focus on determining whether Rop has a unifying
role in polarized plant cell growth, uncovering the mechanistic relationship between Rop and Ca2+, and
understanding how these signaling events are mediated
by specific spatial cues and how they control polarized
secretion and cytoskeletal organization. Clearly, a genetic
approach will continue to provide a new inroad into tip
growth signaling pathways in plants.
Acknowledgements
I am grateful to John Fowler and Desh Pal S Verma for their valuable
comments on the manuscript and to members of my laboratory for helpful
discussions. This work is supported by National Science Foundation and
United States Department of Agriculture.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
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•
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•
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The demonstration that microinjected anti-Rop1Ps antibodies specifically
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Further, the antibody-induced growth inhibition is not associated with
changes in cytoplasmic streaming, whereas growth arrest induced by the
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