Journal of Experimental Botany, Vol. 60, No. 7, pp. 1969–1978, 2009
doi:10.1093/jxb/erp113 Advance Access publication 8 April, 2009
DARWIN REVIEW
Understanding phototropism: from Darwin to today
Jennifer J. Holland, Diana Roberts and Emmanuel Liscum*
Division of Biological Sciences, 109 Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA
Received 28 January 2009; Revised 12 March 2009; Accepted 17 March 2009
Abstract
Few individuals have had the lasting impact on such a breadth of science as Charles Darwin. While his writings about
time aboard the HMS Beagle, his study of the Galapagos islands (geology, fauna, and flora), and his theories on
evolution are well known, less appreciated are his studies on plant growth responses to a variety of environmental
stimuli. In fact, Darwin, together with the help of his botanist son Francis, left us an entire book, ‘The power of
movements in plants’, describing his many, varied, and insightful observations on this topic. Darwin’s findings have
provided an impetus for an entire field of study, the study of plant tropic responses, or differential growth (curvature)
of plant organs in response to directional stimuli. One tropic response that has received a great deal of attention is
the phototropic response, or curvature response to directional light. This review summarizes many of the most
significant advancements that have been made in our understanding of this response and place these recent
findings in the context of Darwin’s initial observations.
Key words: Auxin, Chlodony–Went theory, Darwin, LOV domain, phototropin, phototropism, protein kinase.
‘The power of movements in plants’: Darwin’s lasting legacy to the field of phototropism
research
Plants are sessile by nature, and thus to maximize energy
production they must rely on their capacity to move
directionally, or exhibit tropic responses, in response to
directional environmental cues. The way plants respond to
stimuli has fascinated humans since the time of Ancient
Greece (Whippo and Hangarter, 2006). Although Charles
(and son Francis) Darwin’s ‘The power of movements in
plants’ dealt in large part with Darwin’s proposal that
circumnutation could provide a unifying model to explain
directional growth responses in plants (Darwin, 1880), an
hypothesis that has been shown to be generally incorrect,
this seminal book has provided the foundation for an entire
field of study focused on the tropic responses of plants.
‘The power of movements in plants’ proposed several key
elements that shape the current research on tropic
responses. Darwin, although not the first to do so (for an
excellent historical literature review on tropic response
research, see Whippo and Hangarter, 2006), proposed that
plants could grow differentially (thus directionally) in
response to external stimuli such as light or gravity. Second,
he demonstrated that the part of the plant that perceives the
stimulus is separate and distinct from the part that responds
to that stimulus. In the case of phototropism, directional
light is perceived in the apical portion of a young seedling
and ‘transduced’ to more basally localized portions of the
shoot as a differential signal that informs the plant which
side is the closest to and which is the furthest from the light
source such that a bending response occurs (Fig. 1). Finally,
Darwin proposed that an ‘influence’ (though he was unable
to identify it) moves from the site of stimulus perception to
the area of response where bending occurs (Fig. 1).
Darwin’s ‘influence’: auxin and its role in
phototropism
Just after the turn of the century Boysen-Jensen (1911) was
able to gain further insight into Darwin’s ‘influence’ in an
experiment that used pieces of mica to disrupt the proposed
influence’s flow, and the results of those experiments
confirmed that the ‘influence’ does indeed participate in
a plant’s response to directional stimuli, such as light. In
* To whom correspondence should be addressed: E-mail: [email protected]
ª The Author [2009]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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1970 | Holland et al.
Fig. 1. Stylized representation of phototropism. The diagrams
depicted here are meant to represent the coleoptile of a darkgrown grass seedling, such as oat, which is a classic model for
phototropism. On the left is a seedling soon after exposure to
unidirectional blue light (half sun to the right of the seedling). The
‘eye’ is used to represent Darwin’s proposal that light sensing
occurred within a specific region of the seedling (in this case the tip
of the coleoptile), not that Darwin was ascribing any anthropomorphic properties to the plant per se. The downward pointing black
arrows represent the downward flow of the ‘influence’ (we now
know as auxin) that Darwin proposed moved from the site of light
perception to the site of differential growth that results in curvature.
The horizontal black arrows reflect the lateral movement of auxin
occurring from the lit to the shaded side of the seedling that has
been demonstrated to occur in a variety of plants. On the right is
a seedling that has developed a curvature response after a refractory period (tx) during which the differentially accumulated
auxin (green shading) promotes localized growth (plus signs).
particular, Boysen-Jensen’s experiments suggested that
Darwin’s ‘influence’ flows from the tip of the plant toward
the base in the unlit side of the plant, and that this
directional and differential movement of the ‘influence’ is
critical for the plant’s bending response.
Although textbooks generally credit the Dutch plant
physiologist Fritz Went with the identification on Darwin’s
‘influence’ as the now well-understood plant hormone
auxin, the actual history of auxin’s chemical identification
is a bit more complicated. First, it is important to give
shared credit for the physiological identification of auxin to
the Russian plant physiologist Nicolai Cholodny, who,
while Went was working with grass coleoptiles (Went,
1926), was generating similar results with grass roots
(Cholodny, 1927). It is also critical to note that, in actuality,
it is Kogl and colleagues (Kogl and Haagen-Smits, 1931) at
Utrecht University (where Went did his graduate work) that
deserve credit for the first chemical identification of an
‘auxin’ from human urine. Cholodny (1928) and Went
(1928) each independently proposed a similar mechanism
by which auxin could mediate tropic responsiveness, which
was later simply renamed the Cholodny–Went theory (Went
and Thimann, 1937). In brief, the Choldony–Went theory
combines Darwin’s hypotheses with those of the auxin
pioneers to propose that an asymmetric accumulation of
auxin occurs in response to a tropic stimulus, and that this
asymmetric gradient of auxin stimulates the differential
growth response that results in tropic curvature. While
other models have been proposed, the Cholodny–Went
theory is still the prominent one used to explain a plant’s
response to tropic stimuli.
Following the initial proposal of the Cholodny–Went
theory, a number of hypotheses have evolved regarding how
the unequal distribution of auxin occurs, particularly in
response to phototropic (directional light) stimulation. For
example, Went and Thimann (1937) hypothesized that the
unequal auxin accumulation occurs due to either light
inactivation of auxin on the stimulated side, light-induced
inhibition of the production of auxin, or light-induced transport of the auxin from the lit side to the shaded side. A study
by Briggs et al. (1957) showed that introducing a physical
barrier between the lit and the shaded side of corn coleoptiles
disrupts the formation of an auxin gradient, providing
evidence against the arguments that light induces the destruction, or the inactivation, of auxin. Subsequently, Briggs
(1963) published additional data that provided support for
a hypothesis that the unequal distribution of auxin was due to
a lateral movement or transport of auxin. Specifically, these
data showed that, in maize coleoptiles, an increase in the
amount of curvature in response to light was correlated to an
increase in the amount of auxin present on the ‘shaded’ side
of the coleoptile (Fig. 1).
Pickard and Thimann (1964) applied radio-labelled
auxin, indole-3-acetic acid (IAA) in particular, to maize
coleoptiles to trace the path of auxin during phototropism.
It was found that IAA moves laterally across the coleoptile
from the lit to the shaded side under both the pulse (first
positive) and extended (second positive) irradiation conditions (Fig. 1). Based on similar radio-tracer labelling
studies, Shen-Miller and Gordon (1966) proposed that light
promotes a lateral accumulation of auxin by inhibiting
polar auxin transport. Gardner et al. (1974) obtained
additional support for the notion that light stimulates the
lateral movement of auxin, although their data did not
support a role of light-mediated inhibition of polar auxin
transport.
In recent years, genetic studies in the model plant
Arabidopsis thaliana have identified proteins that appear to
function as auxin transport facilitators (Leyser, 2006). At
least five auxin transport proteins have been associated with
stem/shoot phototropism: AUX1 (AUXIN-RESISTANT 1;
Stone et al., 2008), PIN1 (PIN-FORMED 1; Blakeslee
et al., 2004), PIN3 (Friml et al., 2002), MDR1 (MULTIDRUG-RESISTANT 1), and PGP1 (P-GLYCOPROTEIN
1; Noh et al., 2003). Studies in Arabidopsis have also led to
important findings about how a gradient of auxin established by such transport facilitators leads to differential
growth. For example, semi-dominant loss-of-function mutations in the NPH4 (NON-PHOTOTROPIC HYPOCOTYL
4)/ARF7 (AUXIN RESPONSE FACTOR 7) locus, and
dominant gain-of-function mutations in MSG2 (MASSUGU 2)/IAA19 and AXR5 (AUXIN-RESISTANT 5)/
IAA1 result in severely impaired phototropic and gravitropic responses (Liscum and Briggs, 1996; Watahiki and
Yamamoto, 1997; Stowe-Evans et al., 1998; Harper et al.,
2000; Park et al., 2002; Tatematsu et al., 2004; Yang et al.,
2004). NPH4/ARF7 is a transcriptional activator whose
Phototropism, Darwin to today | 1971
activity is repressed in the presence of the MSG2/IAA19
and AXR5/IAA1 (Liscum, 2002). In the presence of
elevated levels of free auxin, MSG2/IAA19 and AXR5/
IAA1 are rapidly degraded by a 26S proteasome that
requires the SCFTIR1 complex containing the auxin receptor
TIR1 to target these proteins for degradation (Tan et al.,
2007). This, in turn, allows homodimerization of the NPH4/
ARF7 protein and transcription of ‘auxin responsive genes’
(Tatematsu et al., 2004; Celaya et al., 2009). A recent
transcript profiling study in Brassica oleracea has identified
a number of genes that appear to represent targets of
NPH4/ARF7 regulation in response to tropic stimulation;
these include genes encoding proteins involved in the
regulation of free auxin levels, additional transcriptional
regulators, and proteins involved in the regulation of cell
wall extensibility (Esmon et al., 2006).
Darwin’s vision: phototropin blue light
receptors
In addition to proposing the existence of a mobile ‘influence’ that was necessary for tropic responses (we now
know this ‘influence’ to be auxin; see above), Darwin made
observations, again presented in ‘The power of movements in
plants’, that indicated that tropic curvatures in response to
light were not general light responses but specific with
respect to light quality. In particular, Darwin was able to
demonstrate that the blue region of the electromagnetic
spectrum is the most effective portion of the spectrum with
respect to the induction of phototropism. These findings
have, like those of Darwin’s tropic ‘influence’, provided the
impetus for a large number of studies over the past 100 or
so years. Yet only within the past decade or so have the
molecular details of how plants ‘see’ blue light cues (Fig. 1)
to induce phototropism, ‘Darwin’s vision’ if you will, have
become known.
As was the case with the elucidation of the molecular
mechanisms underpinning the role of auxin in phototropism, Arabidopsis genetics was also a major factor in the
identification of the photoreceptor molecules mediating
phototropism in higher plants. The first of these photoreceptors identified at the molecular level is phototropin 1
(phot1) (Huala et al., 1997), originally designated NPH1
(for its non-phototropic hypocotyl mutant phenotype; Liscum and Briggs, 1995). The PHOT2 gene was subsequently
identified based on its high degree of sequence homology to
PHOT1 (Jarillo et al., 2001; Sakai et al., 2001). Phototropins regulate not just phototropism, but a number of
additional blue light responses, including stomatal opening,
chloroplast movements, leaf movements and expansion, and
rapid inhibition of stem growth (Christie, 2007).
The functions of the phototropins in these responses are
both overlapping and distinct. For example, in the case of
phototropism, phot1 (see Briggs et al., 2001, for a description of nomenclature) is the dominant receptor, mediating
response across a wide range of fluence rates (e.g. 0.01–100
lmol m-2 s-1), whereas phot2 appears to operate only at
higher fluence rates (>10 lmol m-2 s-1) (Sakai et al., 2001).
By contrast, with respect to stomatal regulation, both phot1
and phot2 contribute over the entire range of effective fluence
rates (Kinoshita et al., 2001; Kinoshita and Shimazaki, 2002).
The interplay between the phototropins is even more
complex when one considers blue light-induced chloroplast
movements. In high-light conditions, chloroplasts move away
from the upper surface of the leaf to avoid photobleaching
(Wada et al., 2003), a response that is mediated solely by
phot2 (Jarillo et al., 2001; Kagawa et al., 2001). However, in
low light, both phot1 and phot2 appear to contribute equally
to the accumulation of chloroplasts along the upper surface
of the leaf to maximize photosynthetic light capture (Wada
et al., 2003).
PHOT1 and PHOT2, being duplicate genes, encode
proteins that are strikingly similar in their overall sequence
and structure (Christie, 2007). Structurally, the phototropins consist of two major parts: (i) an amino-terminal
photosensory domain, and (ii) a carboxyl-terminal Ser/Thr
protein kinase signalling domain (Fig. 2). Both portions of
the protein are necessary for phototropic signalling and
much has been learned in recent years about how each
portion functions and is regulated, as discussed below.
LOVing blue light: photosensory mechanism of
phototropins
The photosensory domain of a phot contains two ;110
amino acid islands with homology to each other that are
critical for photoreceptor activity (Christie, 2007): LOV1
(light, oxygen, voltage) and LOV2 (Fig. 2). The LOV
domains are members of the larger PAS (Per, Arnt, Sim)
domain superfamily (Huala et al., 1997; Crosson et al.,
2003). Each of the LOV domains binds a single molecule
of blue light-absorbing flavin mononucleotide (FMN)
(Christie et al., 1998), imparting photoreceptor function to
the phototropins (Christie et al., 1999; Salomon et al., 2000).
As shown in Fig. 3, photosensitive LOV domains undergo a unique photocycle in response to absorption of blue
light (Celaya and Liscum, 2005; Christie, 2007; Matsuoka
et al., 2007). In darkness, the FMN chromophore is bound
non-covalently to the LOV domain as a singlet ground state
molecule. This state, which is capable of absorbing blue
light, is referred to as LOVD447 (Salomon et al., 2000;
Fig. 2. Domain organization of the phototropin blue light receptors. Both phototropins (phot1 and phot2) share the same basic
organization with two amino-terminal LOV (light, oxygen, and
voltage) domains and a carboxyl-terminal protein kinase domain.
Although not shown here, a single molecule of FMN (flavin
mononucleotide) is associated with each LOV domain as a lightharvesting cofactor.
1972 | Holland et al.
Fig. 3. Proposed photocycle of the phototropin LOV domains. The photocycle begins with the absorption of a blue photon of light by
the dark-state (LOVD447) and subsequent conversion to an excited singlet state (asterisk). The excited singlet state is then converted to
the red light-absorbing (LOVL660) excited triplet state (T), which is hence converted into the near-UV-absorbing covalent adduct (LOVS390)
that represents the active state. Both the singlet and active LOVS390 states can be converted to the initial dark-state by incubation in
darkness. Details of this photocycle are described in the text. Approximate half-times of reactions are given.
Crosson and Moffat, 2001; Swartz et al., 2001) and
absorption of a single photon of blue light results in the
generation of an excited singlet FMN, which is rapidly
converted into a red-shifted triplet state (LOVL660) (Swartz
et al., 2001; Corchnoy et al., 2003; Kennis et al., 2003;
Kottke et al., 2003). The triplet state flavin rapidly decays to
form a covalent adduct between the C(4a) atom of the
FMN and the cysteine within a highly conserved motif
(GXNRCFLQ) in the LOV domain; a state with a near UVshifted absorption maximum designated LOVS390 (Salomon
et al., 2000; Crosson and Moffat, 2001, 2002; Swartz et al.,
2001; Kasahara et al., 2002; Fedorov et al., 2003; Kennis
et al., 2003; Kottke et al., 2003). This FMN-cysteinyl adduct
is completely reversible in darkness (Salomon et al., 2000;
Swartz et al., 2001; Kasahara et al., 2002; Kennis et al., 2003)
or after absorption of a second near UV photon (Kennis
et al., 2004). Thus, LOV domains cycle between two major
states (with a transient intermediate): the dark state
(LOVD447) and the lit state (LOVS390), depending upon the
light condition.
It is generally accepted that the LOVS390 FMN-cysteinyl
adduct represents the active signalling state of a phototropin
(Crosson et al., 2003; Celaya and Liscum, 2005; Christie,
2007; Matsuoka et al., 2007). Consistent with this model,
replacement of the critical cysteine with either serine or
alanine eliminates the formation of LOVS390 (Salomon et al.,
2000; Swartz et al., 2002; Kottke et al., 2003), and expression
of a PHOT1 transgene containing the cysteine to alanine
mutation in both LOV1 and LOV2, or LOV2 alone, fails to
complement the aphototropic phenotype of a phot1 null
mutant (Christie et al., 2002). It is interesting to note that
a LOV1 cysteine to alanine single mutant transgene does
compliment the aphototropic phot1 mutant phenotype, indicating that the two LOV domains are not equal with respect
to physiological function (Christie et al., 2002; Sullivan et al.,
2008). Similarly, LOV1 is dispensable, whereas LOV2 is
sufficient on its own to mediate function of phot2 in the
chloroplast avoidance response (Kagawa et al., 2004).
The aforementioned findings raise an obvious question:
what is the functional role of the LOV1 domain? Several
independent studies (Salomon et al., 2004; Nakasako et al.,
2004; Katsura et al., 2008), suggest that LOV1 may function
as a dimerization motif; a finding certainly not at odds with
the fact that LOV domains are a sub-class within the larger
PAS domain superfamily (Crosson et al., 2003). It is also
interesting to note that the quantum efficiency for
Phototropism, Darwin to today | 1973
conversion of LOVD447 to LOVS390 is about 10-fold higher
in LOV2 than LOV1 in phot1 (Salomon et al., 2000;
Kasahara et al., 2002; Iwata et al., 2005), although once
photoconverted the LOV1 domain is longer-lived than
LOV2 (Kasahara et al., 2002; Iwata et al., 2005). These
observations suggest that at least in the case of phot1, the
predominant receptor mediating phototropism, the LOV2
domain is considerably more ‘photodynamic’ than LOV1,
and that selective pressures in nature are stronger on LOV2
versus LOV1. It remains to be determined why, if it is not
functioning to regulate phototropin activity, LOV1 remains
photosensitive at all.
Sharing the LOV: protein kinase domain activation
As already mentioned the phototropins contain a Ser/Thr
protein kinase domain in their carboxyl-terminal regions
(Christie, 2007). While no native substrates for the phot
protein kinase domain, other than the phototropins themselves, are currently known (Christie, 2007; Matsuoka et al.,
2007), mutational studies have demonstrated that the
catalytic activity of this domain is apparently necessary for
phototropic signal-output (Christie et al., 2002; Cho et al.,
2007). Because of this latter fact much effort has been
focused in recent years on understanding how the blue lightdependent formation of LOV2S370 leads to activation of the
protein kinase domain.
While initial X-ray crystallography studies suggested that
only minimal changes occur in the tertiary structure of
a LOV domain during photocycling (Crosson and Moffat,
2001, 2002; Fedorov et al., 2003), solution spectroscopy
provided clear evidence that, in fact, the structural rearrangements associated with the formation of LOVS370 are
fairly pronounced, especially if the polypeptides being
examined also encompassed regions carboxyl-terminal to
LOV2 (Swartz et al., 2002; Corchnoy et al., 2003; Eitoku
et al., 2005; Iwata et al., 2005). Nuclear magnetic resonance
(NMR) studies by Harper and colleagues (Harper et al.,
2003, 2004) identified an alpha-helical region (designated
the Ja-helix) that resides between LOV2 and the protein
kinase domain, which, in darkness, associates with the
solvent-exposed surface of the b-sheet portion of the LOV2
core region facing away from the FMN chromophore.
Upon blue light-induced FMN-cystenyl adduct formation
the Ja-helix becomes disordered and dissociates from LOV2
(Harper et al., 2004). A number of mutations were identified
that could mimic the aforementioned ‘dissociated state’ in
the absence of light exposure, and, when introduced into
a full-length phot1, these same mutations resulted in lightindependent autophosphorylation of the phot1 protein,
suggesting that the LOV2-Ja-helix interaction acts to repress the protein kinase activity of phot1 (Harper et al.,
2004). In support of such a LOV2 domain ‘repression
model’ (Fig. 4), in vitro studies have shown that an isolated
protein kinase domain from phot2 is catalytically active
against casein, a common in vitro substrate for protein
kinase assays (Matsuoka and Tokutomi, 2005). These
Fig. 4. ‘Repression domain’ model for photoactivation of the
phototropin protein kinase domain. (A) In darkness the LOV2
domain and cis-associated Ja helix adopt a compressed closed
configuration that appears to repress the activity of the carboxylterminal protein kinase domain. (B) Upon absorption of a photon of
blue light by the non-covalently associated FMN molecule
[conversion of LOV2D447 to LOV2L660 is represented by the
transition from oval FMN in (A) to starred FMN in (B)], the active
cysteinyl-LOV2 domain adduct is formed to induce progressive
structural changes in the LOV2 [represented by the larger blue
LOV domains in (B) as compared to smaller grey LOV domains in
(A)] that result in unfolding of the Ja helix and de-repression of the
protein kinase domain. The active protein kinase domain can then
catalyse the autophosphorylation of phototropin (blue balls with
a P in each) and currently unknown substrates. The positions of
the autophosphorylation sites are generally representative of those
determined experimentally but are not meant to depict precisely
and exclusively those sites.
results further suggest that phototropins may target proteins other than themselves for phosphorylation in planta,
although again no such substrates are currently known.
Moving distances with LOV: intracellular localization of
phototropins is dynamic and light regulated
Movements of the phototropins are not limited to the
angstrom-level intramolecular movements upon formation
of LOVS390, rather the entire phototropin protein appears
to move from one part of the cell to another in response to
blue light. For example, while phot1 is normally tightly
associated with the plasma membrane in dark-grown seedlings, probably through its carboxyl-terminal protein kinase
domain (Kong et al., 2006), blue light induces the relatively
rapid (within minutes) movement of some proportion of
phot1 to intracellular locations (Sakamoto and Briggs,
2002; Wan et al., 2008). Similar relocalization properties
have also been observed for phot2; although the
1974 | Holland et al.
intracellular compartment to which phot2 moves appears to
be the Golgi (Kong et al., 2006). At present it is unknown
exactly how phototropin movement is linked to a particular
physiological response, however, a recent study by Han and
colleagues (Han et al., 2008) suggests that this dynamic
response may be coupled with receptor adaptation/desensitization or signal attenuation. Specifically the authors found
that blue light-induced relocalization of phot1 can be
largely, if not completely, prevented by prior exposure to
red light (Han et al., 2008); light conditions that also lead to
phytochrome A-mediated enhancement of phot1-dependent
phototropism (Stowe-Evans et al., 2001; Han et al., 2008).
Thus it would appear that plasma membrane-localized
phot1 is more ‘active’ in terms of phototropic signalling
than internalized phot1. Certainly the dynamic nature of
phototropin localization represents fertile ground for future
studies.
Getting from Darwin’s vision to his
‘influence’: early phototropin signalling
components
One of the biggest questions currently facing the community
of researchers who study phototropism at the molecular level
is: how does phototropin activation lead to auxin-regulated
differential growth (curvature)? While the details of this
process still remain largely unknown, several components of
this ‘black box’ have been identified, most notably three
phot1-interacting proteins: NPH3 (NON-PHOTOTROPIC
HYPOCOTYL 3; Motchoulski and Liscum, 1999), RPT2
(ROOT PHOTOTROPISM 2; Inada et al., 2004), and
PKS1 (PYTOCHROME KINASE SUBSTRATE 1; Lariquet
et al., 2006).
NPH3 and RPT2 are paralogous proteins that represent
the founding members of the moderately sized NRL
(NPH3/RPT2-Like) protein family (33 members in total) in
Arabidopsis (Celaya and Liscum, 2005; Celaya et al., 2009).
Members of the NRL family, including NPH3 and RPT2,
share five regions of primary sequence conservation (Fig. 5):
DIa (Domain Ia) and DIb, together comprising an aminoterminal BTB (Broad-Complex/Tramtrack/Bric-à-Brac) domain (Aravind and Koonin, 1999; Stogios et al., 2005); DII,
resembling no known structural or functional motif; and the
Fig. 5. Domain organization of the NRL (NPH3/RPT2-Like) family
of proteins. Members of the NRL family, including the founding
members and phototropic signal transduction components NPH3
and RPT2, share five domains of conserved sequence homology
designated DIa to DIV. They also contain two regions of conserved
predicted secondary structure; an amino-terminal BTB domain
(encompassing most of DIa and DIb) and a carboxyl-terminal
coiled-coil (C-C).
remaining two regions, DIII and DIV, together representing
the Pfam ‘NPH3 domain (PF03000)’ of unknown function
(Finn et al., 2008). The NRL family also exhibits several
regions of conserved predicted secondary structure that have
diverged in sequence (Fig. 3); most notably a carboxylterminal coiled-coil (Lupas and Gruber, 2005) that is present
in approximately half of the family members (Celaya and
Liscum, 2005; Pedmale and Liscum, 2007). Although the
functional roles of each of the aforementioned ‘domains’ are
currently not fully understood, the coiled-coil has been
shown to represent the phot1-interaction domain of NPH3
(Motchoulski and Liscum, 1999; Pedmale and Liscum, 2007),
while the BTB domain can mediate interaction between
NPH3 and RPT2, at least in yeast (Inada et al., 2004).
Recent studies have shown that the BTB domain of NPH3
can also mediate interaction with CULLIN 3 (CUL3)
(Pedmale and Liscum, 2007). These latter results suggest that
NPH3 may represent the substrate adapter component of
a CUL3-based E3 ubiquitin ligase, a recently recognized role
for many BTB-containing proteins (Krek, 2003; Pintard
et al., 2004; van den Heuvel, 2004; Willems et al., 2004;
Stogios et al., 2005; Perez-Torrado et al., 2006).
While no target for ubiquitination by an NPH3-CUL3
complex has yet been reported, one can imagine that such
a target might function in the regulation of auxin transport.
Findings that phototropic stimulation fails to induce an
asymmetric distribution of auxin across the coleoptile in the
rice mutant cpt1 (coleoptile phototropism 1) (Haga et al.,
2005) is consistent with this hypothesis. CPT1 encodes the
rice orthologue of Arabidopsis NPH3 (Haga et al., 2005),
thus placing NPH3/CPT1 downstream of phot1 and upstream of the regulation of auxin redistribution. Recent
studies suggest that regulation of auxin transport may
represent a common function of NRL family members. For
example, mutations in the NPY/ENP/MAB4 (NAKED PINS
IN YUC MUTANTS/ENHANCER OF PINOID/MACCHIBOU 4) subfamily of the NRL superfamily appear to
influence auxin-mediated organogenesis through alterations
in auxin movement (Cheng et al., 2007; Furutani et al.,
2007), probably through genetic interactions between the
NPY proteins and the AGC kinases PID (PINOID), PID2,
WAG1 (denotes the ‘wagging’ root growth it mediates), and
WAG2 (Cheng et al., 2008). This latter observation is
particularly intriguing as phot1 is also an AGC kinase
(Bögre et al., 2003; Galván-Ampudia and Offringa, 2007).
The PKS1 protein was originally identified as a negative
regulator of phytochrome signalling and to serve as a substrate for phytochrome’s protein kinase activity (Fankhauser
et al., 1999), but has since been shown to function as
a positive regulator of phototropism as well and physically
to interact with both phot1 and NPH3 (Lariquet et al.,
2006). At present, it is not understood how PKS1 (or PKS2
and PKS4; Lariquet et al., 2006) influences phototropism at
a molecular level, but it is tempting to speculate that the
PKS proteins may bridge the enhancing influences of
phytochrome on phot1-dependent phototropism (Liscum
and Briggs, 1996; Parks et al., 1996; Janoudi et al., 1997;
Stowe-Evans et al., 2001; Liscum, 2002), possibly through
Phototropism, Darwin to today | 1975
influences on phot1 localization (Han et al., 2008). It is also
worth noting that NPH3, like PKS1 (Fankhauser et al.,
1999), is a phosphoprotein whose phosphorylation state and
functional activity is light-dependent; whereas red light
stimulates the phosphorylation of PKS1 in a phytochromedependent fashion (Fankhauser et al., 1999), blue light
results in the desphosphorylation of NPH3 that is dependent
upon the presence of phot1 (Pedmale and Liscum, 2007).
Thus it would appear that the signalling capacity of both
NPH3 and PKS1 are regulated by similar post-translational
mechanisms linked to the photoreceptors through which the
former molecules signal.
phototropic responses, and elucidation of its mechanistic
basis of action; identification of several signalling components functioning between photoperception and auxin responsiveness; and characterization of an adaptive significance
for phototropism under natural growth conditions. However,
the goal remains fully to elucidate all of the molecular
components, from the reception of light to movement, that
contribute to the phototropic response, as well as the
ecological variables that have provided the selective pressures
for the evolution of this response in nature. In all these
regards, there is much work left to do. The next century, like
the last, is likely to bring many answers to such questions,
leading to an even greater appreciation of just how important
‘The power of movements in plants’ really is!
Power of movement meets origin:
phototropism in the field
Though Darwin (1880) hypothesized that phototropic
responses are adaptive to a plant, and this proposal has
been reiterated many times over the past 100 plus years in
one form or another (Iino, 1990; Liscum and Stowe-Evans,
2000; Christie, 2007), it has only been within the last few
years that this hypothesis has actually been experimentally
tested. Galen et al. (2004) have shown that the fitness of
field-grown Arabidopsis plants carrying loss-of-function
mutations in PHOT1 are significantly lower than that of
wild-type plants grown in the same plots. Somewhat
surprisingly, in contrast to previous proposals that stem
phototropism would represent the adaptive response in
nature (Iino, 1990), this study found that root phototropism
was the trait coupled to fitness, and only under high light
conditions (Galen et al., 2004). A subsequent study demonstrated that negative root phototropism (bending away
from directional blue light) enhances the ability of the plant
to access water, which under high light conditions is more
abundant deeper in the soil because of increased evaporation near the surface (Galen et al., 2007a). Three life history
traits in particular were shown to be influenced dramatically
by the ability of a root to access water in arid conditions: (i)
seedling establishment, (ii) accumulation of biomass in
established plants, and (iii) fecundity of plants reaching
adulthood (Galen et al., 2007a). These studies provide an
exciting potential avenue to develop plants capable of
growing in more arid environment that maintain, or even
increase, their production value through genetic engineering
of phot1 signalling (Galen et al., 2007b).
From Darwin to the future: final thoughts
Darwin’s ‘The power of movements in plants’ undoubtedly
stimulated an entire field of study on plant responses to the
environment. Since publication of this seminal work our
understanding of phototropism in higher plants has expanded tremendously. Several significant findings have been
made: identification and characterization of the photoreceptors controlling phototropism; identification of auxin as the
major growth regulator involved in the development of
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