Founders Review
Phototropism: Some History, Some Puzzles,
and a Look Ahead1
Winslow R. Briggs*
Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305
ORCID ID: 0000-0002-3390-0078 (W.R.B.).
Though few and far between, phototropism studies
through 1937 established a number of important principles. (1) Blue light is the active spectral region. (2) The
phototropic stimulus is perceived by the coleoptile tip,
and the consequences of the stimulation progress down
into the growing region. (3) Lateral transport of auxin
mediates the curvature response. (4) The reciprocity law
holds for first positive curvature, whereas second positive curvature is time dependent. (5) Red light treatment had a major effect on phototropic sensitivity. Later
studies established the following. (6) Seven blue light
receptors (cryptochromes, phototropins, and three
F-box proteins) were identified and characterized.
(7) A flavin was established as the photoreceptor
chromophore for all seven. (8) The chromophore domain, designated the LOV domain (for light, oxygen, or
voltage), carries out a unique photochemistry. (9) LOV
domains must be truly ancient chromophore domains.
There remain some puzzles. The fluence-response
threshold level for first positive curvature is far below
that for phototropin photochemistry. Likewise, the
fluence-response threshold level for the red light effect
on coleoptile phototropism is far below those for phytochrome phototransformation. Cytological effects of
red light are also very insensitive compared with the
physiological effects of red light. What is the mechanism
allowing for this extraordinary photosensitivity? How is
phototropin specificity controlled? What are the functions
of the phytochrome kinase substrate proteins in both
phytochrome and phototropin responses? What mechanism leads to lateral auxin transport? Finally, are LOV
domain proteins true photoreceptors in all of the bacteria
in which they occur? If so, what is their biological function?
Even in the ancient world, astute observers noted that
plants could turn to face the sunlight. What was originally designated heliotropism for plants that followed the
sun eventually became divided into two distinct response
categories: solar tracking (the real heliotropism), a repetitive and completely reversible turgor-driven process;
and phototropism, an irreversible directional growth response determined by light direction. Over the past
200 years, a large number of brilliant biologists, including
Julius Sachs (1864), Charles Darwin (1881), Frits Went
1
This work was supported by the National Science Foundation.
* Address correspondence to [email protected].
www.plantphysiol.org/cgi/doi/10.1104/pp.113.230573
(1928), and Kenneth Thimann (Went and Thimann, 1937)
have applied their talents to examining and elucidating
the mechanisms accounting for both of these responses.
The entire history of phototropism and solar tracking
parallels and is intertwined with that for a number of
other blue light responses, found not just in higher
plants but in bryophytes, ferns, algae, fungi, and, most
recently bacteria. For a detailed account of this history,
see Briggs (2006).
Progress in research on blue light-activated processes
over the last half century was severely hampered by a
lack of knowledge of the relevant blue light receptors.
By contrast, the discovery and initial characterization
of a red/far-red-reversible phytochrome (Butler et al.,
1959) nurtured an enormous and sophisticated body of
knowledge about these photoreceptors: their structure,
their chromophores, their photophysics and photochemistry, and the extraordinary signal transduction
networks that they rule. Meanwhile, although a huge
and scattered body of knowledge on blue light responses in plants and fungi accumulated, there was
scarcely a clue to what the photoreceptor(s) might be,
and competing hypotheses abounded. Attention focused on the physical and physiological characterization of responses to blue light and, eventually,
biochemical investigations of intriguing in vitro photochemistry. It was only with the advent of modern molecular genetics and its extraordinary capabilities that
research on blue light photobiology finally began to
catch up with phytochrome photobiology 20 years ago
and the first blue light receptor, cryptochrome1 (cry1),
became identified (Ahmad and Cashmore, 1993).
This review will go back to some of the puzzles of
earlier years, a few over 100 years old, and provide a
glimpse of the status of these puzzles today. They arose
from studies of response kinetics, action spectroscopy,
interactions between blue and red regions of the visible
spectrum, and discrepancies between in vivo and
in vitro results. Although the focus will be on higher plant
phototropism, several other blue light responses will
contribute to the discussion. No effort will be made to be
comprehensive. Any effort here would be redundant
with that of three recent excellent reviews on phototropism (Sakai and Haga, 2012; Christie and Murphy,
2013; Hohm et al., 2013) and on LOV (for light, oxygen,
or voltage) domain photochemistry (Losi and Gärtner,
2011, 2012). The article concludes with a look at the
unexpected role of LOV domains in prokaryotes.
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13
Briggs
WHAT ARE THE KINETIC PROPERTIES OF HIGHER
PLANT PHOTOTROPISM?
Over a century ago, Fröschel (1908) and Blaauw (1909)
first reported that the phototropic responses of Lepidium
spp. seedlings and Avena spp. coleoptiles, respectively,
obeyed the reciprocity law of Bunsen and Roscoe (1862).
The law states that as long as the light dose (fluence:
intensity 3 time) is held constant, a given light response,
in these two cases phototropism, will remain the same
over a broad range of intensity 3 time combinations. In
both cases, the authors were investigating threshold responses, something that later investigators tended to
forget. Meanwhile, du Buy and Nuernbergk (1934) collected data from a number of authors and published the
fluence-response curve shown in Figure 1 for the phototropic responses of Avena spp. coleoptiles over an immense range of fluences (8 orders of magnitude). The
first maximum was designated first positive curvature,
the immediately subsequent minimum first negative
curvature, the second maximum second positive curvature, the next minimum a “zone of indifference,” and
the final ascent third positive curvature. First positive
curvature was usually located only a short distance
below the coleoptile tip, whereas second positive curvature extended somewhat farther down the coleoptiles. For some reason, reciprocity tests were never carried
out at any fluences above the threshold assays used by
Fröschel (1908) and Blaauw (1909), although their conclusions, unfortunately, became accepted and applied to
higher plant phototropism in general. All of this early
work was with white light from a variety of sources, and
the unit of fluence at the time was the meter-candle
second (MCS).
Over 50 years ago, Briggs (1960) finally reinvestigated
the reciprocity relationships of phototropism for maize
(Zea mays) and oat (Avena sativa) coleoptiles over a wide
range of fluences and demonstrated that the reciprocity
law was valid only for first positive curvature but not
for second. In all cases, for fluences above 10,000 MCS,
Figure 1. Fluence-response curve for the phototropic responses of
Avena spp. coleoptiles assembled from the literature by du Buy and
Nuernbergk (1934). From Briggs (1960).
maximum phototropic curvature for both species was
attained after about 20 min of unilateral light stimulus
irrespective of fluence. Indeed, a flashing-light experiment with a total fluence of just over 30,000 MCS
showed that with increasing dark periods but constant
flash duration, maximum curvature for maize coleoptiles was only achieved when the total exposure time,
dark plus light, was 20 min or more.
Zimmerman and Briggs (1963a, 1963b) then developed a kinetic model for the phototropic responses of oat
coleoptiles, based on a detailed series of fluence-response
curves, developing a set of differential equations to describe the various curves. The model for first positive
phototropism involved an initial photoreceptor activation and its subsequent photoinactivation, a two-step
photoresponse. The model they developed for second
positive curvature involved the production of an activated photoreceptor followed by a dark reaction that led
to the curvature response. The model, therefore, incorporated a thermal reaction and hence time dependence
for the response, accounting for the lack of reciprocity. It
also required a second photoreaction that reversed the
first photoactivation.
By the early 1960s, it was well established that first
positive curvature is responding strictly according to firstorder photochemistry: the response is linear with respect
to the log of the number of photoreceptor molecules activated. Like first positive curvature, blue light activation
of phototropin1 (phot1) phosphorylation also obeys the
Bunsen-Roscoe reciprocity law both in vivo and in vitro
(Briggs et al., 2001), consistent with this model. The descent of the response curve following the first positive
maximum is then thought to involve a decrease in the
difference between photoactivation of the photoreceptor
on irradiated versus shaded sides of the coleoptiles. As
fluences are increased, molecules of the photoreceptor on
both sides of the coleoptiles all eventually become photoactivated and the differential disappears. This current
hypothesis does not exactly match the model from
Zimmerman and Briggs (1963b) for first positive phototropism. However, activation of photoreceptor molecules
on the shaded side could replace the photoreceptor inactivation their model requires.
Let us examine the situation for second positive curvature. As exposure time increases, the activated phototropin molecules are postulated to relax gradually to their
dark state and can now be reactivated. As there is a light
gradient across the organ, reactivation is greater on the
illuminated side than on the shaded side of the coleoptiles
and a persistent differential becomes established, leading
to second positive curvature, time dependent because
it depends on the thermal decay rate for the activated
photoreceptors. Again, the precise model of Zimmerman
and Briggs (1963b) is not directly supported, but the differential reactivation of photoreceptors on the irradiated
versus the shaded side of the responding organ could
replace the reverse photoreaction they postulated.
Evidence for light-induced differential phosphorylation of phot1 across unilaterally illuminated oat coleoptiles (Salomon et al., 1997) supports the hypothesis
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Phototropism
that a light gradient leads to a biochemical gradient in
an activated photoreceptor, both for first and second
positive curvature. Differential activation of auxin-induced
gene expression in Brassica oleracea hypocotyls between
irradiated and shaded sides by blue light, activity downstream from light-activated phototropin (Esmon et al.,
2006), likewise supports this hypothesis. Phototropin
phosphorylation has been shown to be required for functional phototropism (Inoue et al., 2008, 2011). Thus, the
time dependence for recovery of phosphorylated phototropin to its unphosphorylated (and physiologically inactive) dark state could account for the time dependence of
second positive curvature. Indeed, the measured capacity
of phot1 to undergo light-activated phosphorylation in
vivo recovers over a period of minutes following a brief
saturating light pulse (Briggs et al., 2001). (A saturating
pulse is one that is thought to activate all of the photoreceptor molecules at once on both irradiated and shaded
sides of the responding organ, a pulse that fails to induce
curvature, the first minimum in the fluence-response curve
for phototropism [for details, see Briggs et al., 2001].) The
recovery of phototropic sensitivity after such a pulse follows roughly the same time course (Briggs, 1960).
Two features of the du Buy and Nuernbergk (1934)
fluence-response curve remain unexplained: first negative
curvature and third positive curvature. First negative
curvature has only been demonstrated for oat coleoptiles,
is lacking for maize coleoptiles, and has never been
reported for dicot seedlings. It remains a puzzle, although
Zimmerman and Briggs (1963b) developed a model,
similar to that for first positive curvature, that provided a
good fit to the data. Third positive curvature might be
explained by the fact that the data sets leading to this
response differed widely in fluence rate and exposure
time used. These differing light conditions could easily
have led to curious anomalies in response to yield an
apparent “third positive curvature.” The longer exposure
times required to achieve these fluences varied, as did the
light sources. Indeed, since 1937, there has been no further evidence for a third positive curvature in any species
investigated. However, first and second positive curvatures appear to be universal among monocot coleoptiles
and dicot seedlings (Fig. 2; Briggs, 1960; Zimmerman and
Briggs 1963a; Chon and Briggs, 1966; Baskin and Iino,
1987; Iino, 2001; Esmon et al., 2006), including Arabidopsis (Arabidopsis thaliana; Konjevic et al., 1989).
There is a distressing feature in attempts to correlate
light-activated phototropin phosphorylation in vivo
with phototropism: the threshold and saturation fluences for blue light activation of first positive curvature
lie between 1 and 2 orders of magnitude below those for
phosphorylation (Briggs et al., 2001). The physiological
response curve is simply not congruent with the photochemical response curve. This apparent paradox is currently unresolved.
HOW DOES RED LIGHT AFFECT PHOTOTROPISM?
Given that blue light activates phototropic curvature
and red light normally does not (but see below), a
Figure 2. Fluence-response curve for the phototropic responses of
maize coleoptiles. From Briggs (1960).
majority of the early phototropism studies depended on
red light as a safelight. However, Curry (1957) noted for
the first time that small fluences of red light actually
reduced the phototropic sensitivity of oat coleoptiles in
the first positive curvature range by 1 order of magnitude. Zimmerman and Briggs (1963a, 1963b) confirmed
this dramatic effect both for first positive curvature (and
for first negative curvature) of oat coleoptiles and demonstrated in addition that red light had the opposite
effect on second positive curvature: it increased its sensitivity by a factor of 3. Chon and Briggs (1966) reported
similar results with maize coleoptiles. Chon and Briggs
(1966) also demonstrated that the maize response to red
light was fully far-red reversible and appeared to be a
classic phytochrome response.
There is a problem with a simple interpretation of the
results based on phytochrome. Quantitative experiments
with maize coleoptiles led to a surprising finding: Briggs
and Chon (1966) measured fluence-response relationships for the red light effect on first positive phototropism and compared it with those relationships for
phytochrome transformation in vivo for maize coleoptiles. Surprisingly, phototropism was altered by fluences
of red light 3 orders of magnitude too low to cause
measureable phototransformation of phytochrome
(Fig. 3). This discrepancy parallels the paradox in phototropism: blue light induces phototropic curvature at fluences far below those that induce detectable phototropin
phosphorylation either in vitro or in vivo (see above).
This result is all the more paradoxical in that the red
light effect on phototropism is fully far-red reversible if
the far-red light exposures are sufficiently short. (Longer
far-red exposures themselves caused the same shift in
phototropic sensitivity that red exposures did.) These
highly sensitive responses were later designated “very
low fluence” responses (see Mandoli and Briggs, 1981,
who used slightly different terminology). This apparent
paradox is also currently unresolved.
The situation in Arabidopsis is somewhat different.
Red light actually sensitizes both first and second positive curvature. Janoudi and Poff (1991) first showed that
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Briggs
red light treatment enhanced phototropic curvature in
the first positive range, subsequently confirmed and
shown to be mediated by phyA (Hennig, 1996; Parks
et al., 1996). Janoudi et al. (1992) showed that red light
pretreatment actually shortened the lag period between
the start of blue light irradiation and the onset of curvature, again an enhancement. Whippo and Hangarter
(2004) demonstrated that the role of phytochromes was
more complex and that phyB and phyD could also
mediate the sensitization of Arabidopsis phototropism
to higher blue light fluences (for further details, see Han
et al., 2008). To date, there is no evidence for opposite
effects of red light on first and second positive curvature
in Arabidopsis.
Another effect of red light on etiolated coleoptiles
might be related to red light-induced changes in phototropic sensitivity. Briggs (1963a) found that continuous
red light treatment of etiolated maize coleoptiles reduced
the amount of diffusible auxin that could be collected in
agar blocks to roughly one-half of that from dark controls. The decrease was gradual, reaching a stable lower
level after about 2 h. During a dark period after a 2-h red
light pretreatment, the diffusible auxin yield gradually
returned to the dark level, again over a recovery period
of about 2 h. The time courses for these auxin changes
were essentially parallel to the red light-induced decrease in phototropic sensitivity (2 h) and its subsequent
recovery in the dark (2 h).
More recently, studies with phot1 tagged with GFP
provided one possible mechanism for the red lightinduced increase in phototropic sensitivity found in etiolated Arabidopsis hypocotyls. Sakamoto and Briggs
(2002) first noted that blue light induced the movement of
phot1-GFP from the plasma membrane into the cytoplasm, a response explored in detail by Wan et al. (2008).
The response required 10 to 15 min to go to completion.
Subsequently, Kong et al. (2006) reported a similar
movement of phot2-GFP from the plasma membrane in
Arabidopsis hypocotyl cells. Han et al. (2008) then found
that red light given prior to phototropic induction almost
completely eliminated the blue light-induced movement
of phot1. The photoreceptor remained closely associated
with the plasma membrane. Given that lateral auxin
Figure 3. Fluence-response curve for the phototropic curvature of
maize coleoptiles (left) and for phytochrome phototransformation in
vivo (right). From Briggs and Chon (1966).
transport is certain to be associated with plasma membrane proteins, retention of a blue light receptor following
red light treatment could well account for the observed
sensitization of phototropism in Arabidopsis. Interestingly, this red light effect could only be observed in the
actively growing region of the hypocotyls.
While the above mechanism may be valid for the red
light-induced sensitization observed for Arabidopsis, it
can hardly be the whole story. First, red light dramatically desensitizes coleoptiles in the first positive curvature range, rather than sensitizing them. Second, while
first positive curvature loses sensitivity, second positive
curvature gains it. Third, the threshold for this red light
effect in coleoptiles is far below that reported by Han
et al. (2008) for inducing the changes in phot1 subcellular
relocalization in Arabidopsis (Briggs and Chon, 1966).
Thus, the proposed mechanism, retention of phototropin
at the plasma membrane, is clearly not the whole story.
For the third time, an apparent discrepancy between
physiology and photochemistry remains unresolved.
Newman and Briggs (1972) reported that red light
treatment increased the electrical potential between the
top 1 cm of etiolated oat coleoptiles by about 6 mV (with
respect to a reference electrode in a 10 mM KCl solution
containing the roots). The increase began about 10 s after
the onset of red light and recovered to the dark level after
about 6 min (Fig. 4). At that time, a pulse of far-red light
led after about 15 s to a decrease in potential of about
10 mV followed by dark recovery over several minutes.
A second red light pulse had no effect if there had not
been an intervening far-red light pulse. These electrophysiological changes are clearly phytochrome mediated
and indicate some sort of rapid action at the plasma
membrane. Haupt (1959, 1960) some years earlier had
done his classic experiments with the alga genus Mougeotia, demonstrating red/far-red-reversible effects on
chloroplast movement that could only be explained by
parallel-oriented phytochrome molecules in close proximity to the cell surface. Most recently, Jaedicke et al.
(2012) have demonstrated an association of phytochrome
with phototropin at the plasma membrane in protonemata of the moss Physcomitrella patens. They also used a
split yellow fluorescent protein assay to demonstrate an
association of Arabidopsis phytochrome with Arabidopsis
phototropin when they were both injected into onion
(Allium cepa) epidermal cells, although they failed to obtain evidence for such an association in a yeast two-hybrid
test. Hughes (2013) has recently written a comprehensive
review on cytoplasmic signaling mediated by phytochrome, covering the early history as well as recent developments. Work on the phytochromes and their signal
transduction pathways has in recent years focused overwhelmingly on their effects on transcription (Franklin and
Quail, 2010; Quail, 2010; Leiver and Quail, 2011; Zhong
et al., 2012). It is timely that attention is being returned to
possible roles of phytochromes at the plasma membrane.
In 2006, Lariguet et al. (2006) reported an important
finding: the Arabidopsis PHYTOCHROME KINASE
SUBSTRATE1 (PKS1) protein, strongly induced by blue
light but phyA dependent, interacts both in vivo and
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Phototropism
Figure 4. Red (R)/far-red (FR)-reversible changes in potential (mV)
between the top 1 cm of an oat coleoptile and a reference electrode in
a 10 mM solution around the roots. After Newman and Briggs (1972).
in vitro with phot1 and NONPHOTOTROPIC HYPOCOTYL3 (NPH3). Like phot1 and NPH3, PKS1 is plasma
membrane localized. PKS1 also was shown to regulate
root phototropism and root gravitropism (Boccalandro
et al., 2008). A second family member, PKS2, was observed to regulate both leaf flattening and leaf positioning, two phototropin-dependent responses (de Carbonnel
et al., 2010). Finally, Kami et al. (2012) showed that some
nuclear signaling involving phyA is needed for a maximal phototropic response. Thus, the two PKS proteins
may well provide the missing link between phytochrome
and phot1, a link that strongly impacts phototropism.
We are still left with the large discrepancy between
physiology and photochemistry, regardless of mechanism. However, it is possible that the discrepancies
observed between the photosensitivity of phytochrome
phototransformation and both phototropic sensitivity
changes and phototropin phosphorylation could be
explained by some trigger mechanism at the plasma
membrane, an amplification mechanism somehow already charged. This mechanism could be fired when
only a very few photoreceptor molecules are activated.
Such a mechanism might be analogous to the visual
system where a very few photons are sufficient to
activate signaling in a dark-adapted mammalian eye
(Pelli, 1990).
AUXIN DISTRIBUTION AND PHOTOTROPISM
Frits Went (1928) originally proposed that the phototropism of coleoptiles was mediated by light-induced
lateral transport of auxin, a conclusion based on measurements of diffusible auxin from irradiated and shaded
sides of coleoptile tips. Because the total auxin recovered
was less than that from dark controls, however, differential inactivation of auxin, higher on the irradiated side
than on the shaded side, was not eliminated as a potential mechanism leading to curvature. The auxin
mechanism in coleoptiles remained controversial until
Briggs et al. (1957) demonstrated that an impermeable
barrier (a coverslip) placed between shaded and irradiated halves of split maize coleoptile tips eliminated any
auxin differential without affecting overall auxin yield,
confirming Went’s result and conclusion. Briggs (1963b)
and Pickard and Thimann (1964), who used radiolabeled
auxin, confirmed and extended these observations.
Several somewhat more recent studies have demonstrated that the growth differential between irradiated
and shaded sides of phototropically curving organs is
compensatory: a decrease in growth rate on the irradiated side is matched by an increase in growth rate on the
shaded side. Iino and Briggs (1984) documented this
response in maize coleoptiles, and Baskin et al. (1985)
further resolved it with high-resolution time-course
measurements of coleoptiles as curvature developed.
Baskin (1986) then demonstrated a similar compensatory
growth differential in phototropically stimulated epicotyls of pea (Pisum sativum). All three of these studies
are consistent with a model that involves lateral transport of auxin without any net loss or gain of the hormone
itself during the response.
As is well known, Darwin (1881) first demonstrated
the importance of the grass coleoptile tip in perceiving
the phototropic light stimulus. The coleoptile tip itself
had to be irradiated in order for curvature of the lower
regions of the coleoptile to develop curvature. Sierp and
Seybold (1926) and Lange (1927) narrowed the photosensitive region to a fraction of 1 mm of the extreme
coleoptile tip. Boysen-Jensen (1928) then demonstrated
that physical contact between the illuminated and
shaded sides of the oat coleoptile was also essential in
order to obtain phototropic curvature. When he slit the
coleoptile tip and inserted a piece of foil (opaque) or a
chip of glass (transparent) into the slit prior to unilateral
illumination at right angles to the slit, curvature development was blocked. If the slit was parallel to the direction of light, curvature developed even with the
insertion of the barrier. Finally, if he split the tip and
pushed the two halves back together without any barrier, he obtained curvature. Briggs (1963b) repeated the
slit-tip experiment with maize coleoptiles using a glass
barrier and obtained a similar result. When the barrier
was oriented at right angles to the incident light, second
positive curvature was significantly reduced and first
positive curvature was completely eliminated. Briggs
(1963b) then showed that with only 0.5 mm of 5-mm
coleoptile tips intact, unilateral light still induced as great
a differential in diffusible auxin between illuminated and
shaded sides of 5-mm coleoptiles tips as when the apical
4 mm of the 5-mm coleoptile tips was intact. More recently, Palmer et al. (1993) showed that the apical 1 mm
of maize coleoptiles showed the highest level of lightactivated phosphorylation of what was subsequently
identified as phot1.
All of these results indicate for phototropism (1) that
photoperception in the coleoptile apex is essential,
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Briggs
(2) that cell-cell lateral communication between lighted
and shaded sides is essential, and (3) that a phototropin
is likely the photoreceptor. These three conclusions
appear to be unambiguous. Unfortunately, the large
discrepancy between the fluence for threshold phototropism and the fluence for threshold blue light-driven
phototropin phosphorylation casts something of a pall
over the “unambiguous” conclusion implicating a phototropin in coleoptiles.
The growth measurements (Baskin, 1986) demonstrating compensatory growth on irradiated and shaded sides
of pea epicotyls clearly established that lateral transport of
auxin could be functioning in dicots as well as monocots.
In addition, as mentioned above, Esmon et al. (2006)
demonstrated a difference in auxin-activated transcription
between irradiated and shaded sides of B. oleracea hypocotyls. In the past decade, a great deal of information has
accumulated about the several proteins involved in auxin
transport (Sakai and Haga, 2012; Christie and Murphy,
2013). However, an unanswered question remained: is
the site of perception of the light signal in the responding
tissue itself or, as in coleoptiles, is it perceived in the upper
nonelongating tissues and transported basipitally, as in
the case of coleoptiles? Christie et al. (2011) used darkadapted deetiolated Arabidopsis carrying the DR5rev:
GFP reporter protein, a system that responds visually to
auxin, to address this question. They found that unilateral
blue light induces, first, an inhibition of the flow of auxin
from the cotyledons into the vascular tissue and epidermis below, accompanied by an inhibition of growth.
Lateral displacement of auxin into the shaded epidermis
above the elongation zone followed, and the auxin differential generated between epidermis on irradiated and
shaded sides moved down into the elongation zone, accompanied by the development of curvature. Although
blue light-induced inhibition of the auxin efflux transporter ABCB19 accounted for the initial growth inhibition, which auxin transporter(s) are involved in the actual
lateral transport is not currently known. However, the
model developed over a century ago by Darwin for coleoptiles is evidently also valid for Arabidopsis and likely
for other dicots: light perception above the growing tissue
and generation by lateral transport of an auxin gradient
that moves down into the growing tissue.
WHAT CHROMOPHORE DETECTS THE
BLUE LIGHT?
At the beginning of the 19th century, Sebastiani
Poggioli (1817) first asked what color of light was responsible for inducing plant movements. He noted that
the leaves of Mimosa pudica favored violet light for inducing a change in leaf orientation to place the lamina
at right angles to the light source (heliotropism or solar
tracking), likely the first hint that there might be a
specialized photoreceptor that required “violet” light
for its activation and downstream signaling. Some years
later, Payer (1842) demonstrated that true phototropism
of watercress (Nasturtium officinale) seedlings was also
maximally sensitive in the blue region of the spectrum.
Other workers followed with more detailed studies
(Briggs, 2006), but it took until the middle of the 20th
century for Shropshire and Withrow (1958) and Thimann
and Curry (1960) to publish the first definitive action
spectra for first positive curvature of oat coleoptile,
covering the wavelength range 330 to 550 nm. Everett
and Thimann (1968) then produced an action spectrum
for second positive curvature that covered activity over
the same wavelength range.
In subsequent years, action spectra for phenomena
activated by blue light proliferated, with spectra for responses as diverse as phototropism in the two fungi
Phycomyces blakesleeanus and Pilobulus kleinii, phototaxis
in Euglena gracilis, stimulation of carotenoid synthesis by
the fungi Neurospora crassa and Fusarium aqueductuum,
chloroplast rearrangement in the moss Funaria hygrometrica, suppression of a circadian rhythm of conidiation
in N. crassa (Sargent and Briggs, 1967), and several other
phenomena (Presti and Delbrück, 1978). The general
features of all of these action spectra were similar: a
single broad band of activity in the UV-A near 360 nm, a
more complex band in the blue with a maximum near
450 nm, and fine structure indicative of different vibrational modes of the photoreceptor.
Baskin and Iino (1987), using the Okazaki Large
Spectrograph, produced with alfalfa (Medicago sativa)
seedlings what remains technically the best action spectrum by far for first positive phototropism. It extends
from 530 nm well into the UV-B region of the spectrum
(down to 260 nm) and documented for the first time a
peak of activity around 280 to 290 nm, about one-third as
high as the 450-nm maximum. Their action spectrum
coincided almost exactly with that obtained by Thimann
and Curry (1960) for oat coleoptiles over the entire wavelength range covered by both studies.
Conventional wisdom for many decades was that there
was a single blue light receptor common to all of these
responses. The overriding controversy was whether the
chromophore was a carotene, a flavin, or something entirely different. It was only in 1993 that the first blue light
receptor was identified, cry1 in Arabidopsis (Ahmad and
Cashmore, 1993). Lin et al. (1995) soon identified a second
cryptochrome (cry2). The cryptochromes are structurally
related to DNA photolyases, two-chromophore proteins
involved in DNA repair and binding both a flavin and
either a pterin (methenyltetrahydrofolate) or a deazaflavin as chromophores (Sancar, 2003). Cryptochromes
were found to bind a flavin and most likely methenyltetrahydrofolate as the second chromophore (Lin et al.,
1995; Malhotra et al., 1995), an initial win for flavins.
After the discovery of the cryptochromes, identification of the photoreceptor chromophore for phototropism remained controversial. Quiñlones and Zeiger
(1994) proposed that the carotinoid zeaxanthin, an important component of the photoprotective xanthophyll
cycle for photosynthesis, might be the functioning
chromophore for phototropism in maize coleoptiles.
However, Palmer et al. (1996) found that the coleoptiles
of maize seedlings grown on the inhibitor of carotenoid
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Phototropism
biosynthesis norflurazon showed normal phototropism
in the absence of any detectable carotenoids. Ahmad
et al. (1998) then presented evidence that cryptochromes
themselves might be carrying out the photoreceptor
function for phototropism. Lascève et al. (1999) then investigated the stomatal opening responses to both blue
light and phototropism in Arabidopsis mutants in
cryptochromes (cry1, cry2, and a cry1 cry2 double mutant), a blocked xanthophyll cycle mutant (npq1), and the
recently discovered phot1 mutants nph1, nph3, and nph4
(Liscum and Briggs, 1995, 1996). As only the nph mutants suppressed first positive phototropism in response
to blue light (Liscum and Briggs, 1996; Lascève et al.,
1999), the authors ruled out members of the xanthophyll
cycle and both cryptochromes for phototropism.
Lascève et al. (1999) also eliminated phot1 as mediating
stomatal opening because the phot1 (nph1) mutants
showed significant stomatal opening in the absence of a
phototropic response. Thus, they concluded that there
must be a minimum of four different blue light receptors
in this model species: two cryptochromes, phot1, and an
unknown photoreceptor that functioned for stomatal
opening but not phototropism. The source of this error is
now obvious. The less sensitive phot2 (Jarillo et al., 1998;
Kagawa et al., 2001) had not been identified at the time.
Lascève et al. (1999) had used a fluence rate in the stomatal studies that was high enough to activate phot2,
whereas the fluence they used for the phototropic studies
was much too low to activate phot2 (Sakai et al., 2001).
Hence, they missed phot2’s contribution to phototropism
but detected it for stomatal opening. Thus, the fourth blue
light receptor has turned out to be another phototropin,
phot2, and not a completely different molecule.
Currently unanswered is what the photoreceptor is for
the UV-B peak described by Baskin and Iino (1987). It
could be the consequence of photoexcitation of the UV-Babsorbing peak of the flavin chromophore of one or both
phototropins or of one or more aromatic residues in a
currently unknown photoreceptor protein. It could also
be the consequence of the photoexcitation of UVR8, a
recently described UV-B photoreceptor in Arabidopsis
(Rizzini et al., 2011). Time will tell.
Finally, there have been two reports of phytochromemediated phototropism. Iino et al. (1984) reported very
weak phototropic curvatures of maize mesocotyls. It
could be significantly enhanced by placing the seedlings
horizontally on a clinostat to eliminate curvature elicited
by gravitropism. Red light from above prior to unilateral
red light completely eliminated the phototropic response,
leading the authors to conclude that the photoreceptor
was a phytochrome. Likewise, Parker et al. (1989) observed a weak phototropic response to unilateral red light
from etiolated pea epicotyls that had developed in complete darkness. They reported a sharp decrease in overall
growth rate about 15 min after the onset of red light and
hypothesized that the curvature was the consequence of
differential growth inhibition across the mesocotyl.
Red light from above also eliminated the response,
leading the authors to the same conclusion. It appears
that a phytochromobilin chromophore functions for a
photoreceptor for phototropism, although phototropism is hardly its major assignment.
FINALLY, A PHOTORECEPTOR PROTEIN FOR
PHOTOTROPISM: A SHORT SUMMARY
Identification of the phototropins finally became feasible
with the use of Arabidopsis mutants that were deficient in
phototropism (Khurana and Poff, 1989). Reymond et al.
(1992) found that one of the mutants of Khurana and Poff
(1989), JK224, was severely impaired in its light-inducible
phosphorylation. Liscum and Briggs (1995) then isolated
a phototropism mutant designated nph1 that failed to
respond to unilateral light in the first positive curvature
range and lacked the light-activated phosphorylation reaction. Huala et al. (1997) then used this mutant to identify
and sequence the gene encoding the protein that was the
substrate for light-induced phosphorylation of a membrane protein. It contained two domains about 100 amino
acids long with very similar amino acid sequences, which
they designated LOV domains (as they were similar to
domains in other proteins that were sensitive to light,
oxygen, or voltage). Downstream was a protein kinase
domain, a member of the AGC-VIIIb protein kinase subfamily (Bögre et al., 2003). A year later, Christie et al. (1998)
expressed the gene in insect cells and demonstrated (1) that
it bound a flavin and (2) that light activated its phosphorylation in the absence of any other plant proteins.
These authors thus concluded that it was a photoreceptor
for phototropism. Christie et al. (1999) then demonstrated
that the LOV domains were both binding sites for FMN.
It was not long before a second phototropin, phot2, was
identified (Jarillo et al., 1998; Kagawa et al., 2001).
As we now know (see below), there is a third family of
blue light receptors in Arabidopsis, the Zeitlupe family
(ZTL [Somers et al., 2000], LKP2 [Schultz et al., 2001],
and FKF1 [Nelson et al., 2000]). Rather than playing a
role in phototropism, they are involved in modulating
circadian rhythms and flowering through posttranslational regulation (Fujiwara, 2008). These proteins are all
F-box proteins that use the same unique LOV domain
photochemistry now elucidated for the phototropins and
many bacterial blue light receptors (Losi and Gärtner,
2012). As both cryptochromes, both phototropins, and all
three F-box proteins use a flavin as chromophore, the
long, drawn-out carotenoid versus flavin controversy
has been settled unanimously in favor of flavins. Furthermore, a putative single blue light receptor has now
disintegrated into seven demonstrable blue light receptors: two cryptochromes (possibly a third), two phototropins, and three F-box proteins.
PHOTOTROPIN-MEDIATED SIGNAL
TRANSDUCTION PATHWAYS:
FIERCELY INDEPENDENT?
There is a surprising disconnect between the elements identified for one phototropin-activated signal
transduction pathway and another. For example, the
Plant Physiol. Vol. 164, 2014
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Briggs
protein phosphatase PP2A A1 is required to dephosphorylate (and hence deactivate) phot2 but evidently
plays no role in the dephosphorylation of phot1 (Tseng
and Briggs, 2010). The 14-3-3 l protein isoform is required for optimal stomatal opening mediated by phot2
but has no effect on stomatal opening mediated by
phot1. Furthermore, a mutation at the 14-3-3 l site fails
to affect phot2-mediated phototropism, leaf flattening, or
chloroplast movement (Tseng et al., 2012). Only phot1
mediates the rapid inhibition of stem growth of etiolated
seedlings (Folta and Spalding, 2001). Both the chloroplastavoidance response and nuclear positioning are regulated
only by phot2 (Demarsy and Fankhauser, 2009). Thus,
although many responses can be activated by either
phototropin, perhaps with different sensitivities, many
others depend exclusively on only one of the two photoreceptors. Furthermore, even for a single phototropin,
signal transduction pathways for different responses
must actually differ at the level of the photoreceptor. A
phototropin-interacting protein required for one response
is completely dispensable for another response. For discussion of these and several other examples, see Demarsy
and Fankhauser (2009).
LOV DOMAINS: CHROMOPHORE DOMAINS WITH
A UNIQUE PHOTOCHEMISTRY
Purified LOV domains have provided a rich new
source of material for investigating chromophore structure and photophysics. Salomon et al. (2000) demonstrated that they carried out a unique photoreaction: the
formation of a covalent bond between a highly conserved
Cys and the C-4a carbon of the FMN to form a cysteinyl
adduct. Swartz et al. (2001) first reported that the LOV
domain photocycle involved the formation of a flavin
triplet intermediate prior to cysteinyl adduct formation.
Swartz et al. (2002) also reported protein and chromophore structural changes induced by light using Fouriertransform infrared spectroscopy. Corchnoy et al. (2003)
showed next that LOV domain photoactivation led to
about a 30% decrease in a-helicity, based on circular dichroism measurements. Harper et al. (2003) then showed
that adduct formation led to an unfolding of an amphipathic a-helix just C terminal from the downstream
LOV domain, likely the step necessary to activate the
C-terminal kinase domain (likely accounting for the
a-helicity loss reported by Corchnoy et al. [2003]). A
number of LOV domain structures have now been solved
by x-ray crystallography. Readers should consult the reviews by Möglich et al. (2010) and Losi and Gärtner
(2011, 2012) for a summary of progress in this active area.
SOME FINAL THOUGHTS
Although incredible progress has been made in the
past two decades in understanding plant blue light
receptors and the processes they regulate, there remain
a few puzzles that have stubbornly resisted solving to
date or have been almost totally ignored. The huge
discrepancy between the amount of light that activates
a particular physiological response and the amount that it
takes to activate the responsible photoreceptor is still
unexplained. Indeed, even when a great deal is known
about the activation and relaxation of a photoreceptor, be
it a phototropin or a phytochrome, the discrepancy persists unexplained. Is there a specialized trigger mechanism? (The phytochrome community is actually worse off
than the phototropin community. Their discrepancy has
the physiology and photochemistry separated by about
3 orders of magnitude, whereas the phototropin community must only cope with a discrepancy of somewhere
between 1 and 2 orders of magnitude.) How is phototropin specificity regulated? What determines why a
given response is mediated by phot1 alone, phot2 alone,
or both phototropins? What determines whether a protein
plays a role in one signaling pathway but not another? Do
different sites or patterns of phototropin phosphorylation
play a role? Are there other posttranslational modifications that lend specificity? How does unilateral light
really activate the lateral transport of auxin? What
auxin transporters are involved? These fascinating questions should keep inquisitive plant biologists busy for a
long time.
POSTSCRIPT: LOV BEYOND THE PLANT KINGDOM
Since the original discovery of flavin-binding LOV
domains in phototropins (Christie et al., 1999) and of
their unique photochemistry, light-activated formation
of a flavin-cysteinyl adduct (Salomon et al., 2000), putative LOV domains have been identified in proteins not
only from fungi (Idnurm et al., 2010) but in proteins
from over 10% of all bacteria thus far sequenced (Losi
and Gärtner, 2012; Pathak et al., 2012). The first functional fungal photoreceptor to be characterized was
White collar1 (Wc1) from N. crassa (Froehlich et al.,
2002), and homologs of Wc1 are now known from all
major groups of fungi (Idnurm et al., 2010), including
P. blakesleeanus (Idnurm et al., 2006), the sporangiophores of which were the subject of decades of phototropism research. Wc1 binds the promoters and regulates
the transcription of a number of light-regulated genes in
a blue light-dependent fashion.
The first bacterial protein reported to have a LOV
domain was a LOV-STAS protein, YtvA, from Bacillus
subtilis (Losi et al., 2002). Putative LOV domains are
found upstream from a large number of His kinases
(LOV-HK), the commonest LOV proteins, cyclic-di-GMP
domains (GGDEF; EAL domains), STAS domains, DNAbinding domains, and phosphatase domains. There are
also many short LOV proteins with no known function
(Krauss et al., 2009). Recent metagenome-based screening, largely from the Sargasso Sea but also from the open
ocean, resulted in the assignment of 578 putative LOV
domains on the basis of a highly conserved core region, a
minimum of 14 amino acids thought to be essential for
photoactivity, and a minimal length of 80 amino acids
(Pathak et al., 2012).
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Phototropism
There is a vast reservoir of proteins harboring LOV
domains in nonphotosynthetic as well as photosynthetic
bacteria. (In addition to proteins containing LOV domains, there are many that contain putative phytochromes or BLUF [for blue light sensing using FAD]
domain proteins. Indeed, some bacteria carry two different types of putative photoreceptors and some even
carry three [Gomelsky and Hoff, 2011].) Whenever it has
been possible to express either the LOV domain itself
or the entire LOV protein, they all show normal LOV
domain photochemistry: cysteinyl adduct formation on
photoexcitation. However, a major question remains:
what are the functions of these many putative LOV domain photoreceptors? Finding a phenotype has been a
challenging task. However, in a number of recent cases,
the efforts have been successful. Light activation of a
LOV domain HK in the animal pathogen Brucella abortus
increases its virulence 10-fold in a macrophage assay
(Swartz et al., 2007). Light induces the activity of a cyclic
di-GMP phosphodiesterase activity in the cyanobacterium Synechococcus elongatus (Cao et al., 2010). Light activates a general stress response through the LOV-STAS
protein YtvA in B. subtilis (Avila-Pérez et al., 2006).
A LOV-HK mediates host colonization by the plant
pathogen Xanthomonas axonopodis pv citri (Kraiselburd
et al., 2012). Likewise, a LOV-HK enzyme mediates lightactivated cell attachment for Caulobacter crescentum (Purcell
et al., 2007). A LOV-HK mediates exopolysaccharade
production, attachment, and nodulation in Rhizobium
leguminosarum (Bonomi et al., 2012). Light plays an important role in regulating swarming motility in Pseudomonas syringae through a LOV-HK, a response that also
involves a bacterial phytochrome (Wu et al., 2013). Finally
a LOV-STAS protein confers light-dependent transcription,
swimming motility, and invasiveness to the animal
pathogen Listeria monocytogenes (Ondrusch and Kreft,
2011). This list will no doubt increase.
While information on the signal transduction pathways
that these LOV proteins activate is still scant, it is clear that
there is a whole rich world of bacterial photophysiology
wide open for investigation. Thus, basic research on plant
photoreceptors not only still poses tantalizing questions
about plant photoreceptors themselves but has uncovered
an exciting new field for microbiologists.
ACKNOWLEDGMENTS
I thank Drs. Tong-Seung Tseng and Rajnish Khanna for their careful review
of the manuscript and Dr. Tseng for help in scanning and improving the
quality of published figures. I also thank Michael R. Blatt for providing the
motive farce for this article.
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