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First published online June 13, 2008
Journal of Experimental Biology 211, 2134-2143 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.009365
Effects of exogenous thyroid hormones on visual pigment composition in coho salmon (Oncorhynchus kisutch)
1 Department of Biology, University of Victoria, Victoria, British Columbia,
Canada
2 Department of Microbiology and Biochemistry, University of Victoria, Victoria,
British Columbia, Canada
3 Faculty of Education Research, University of Victoria, Victoria, British
Columbia, Canada
4 Department of Biology and Center for Neuroscience Studies, Queen's University,
Kingston, Ontario, Canada
* Author for correspondence (e-mail: craig.hawryshyn{at}queensu.ca)
Accepted 23 April 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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max) of rods using microspectrophotometry
(MSP). Exogenous thyroid hormone resulted in a long-wavelength shift in rod,
middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) cone
photoreceptors. Rod and LWS cone max values increased,
consistent with an increase in vitamin A2. MWS cone
max values increased more than predicted for a change in
the vitamin A1/A2 ratio. To account for this shift, we
tested for the expression of multiple RH2 opsin subtypes. We isolated and
sequenced a novel RH2 opsin subtype, which had 48 amino acid differences from
the previously sequenced coho RH2 opsin. A substitution of glutamate for
glutamine at position 122 could partially account for the greater than
predicted shift in MWS cone max values. Our findings fit
the hypothesis that a variable vitamin A1/A2 ratio
provides seasonality in spectral tuning and/or improved thermal stability of
visual pigments in the face of seasonal environmental changes, and that
multiple RH2 opsin subtypes can provide flexibility in spectral tuning
associated with migration–metamorphic events.
Key words: rhodopsin, porphyropsin, thyroxine, fish, vision, opsin gene sequence, expression, PCR, MSP
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Bowmaker, 1995).
Visual pigments (VPs) comprise two components: an opsin protein and a
chromophore. Specific amino acid sites throughout the opsin protein play key
roles in spectral tuning of the resultant VP
(Yokoyama, 2000;
Yokoyama et al., 2007). There
are five classes of vertebrate opsins that are categorized based on amino acid
sequence and on spectral absorbance (reviewed in
Bowmaker, 1995;
Yokoyama, 2000). In addition
to expressing a representative of one or more of each of these opsin classes,
some fishes have recently been found to express different subtypes of the
various opsin classes (Chinen et al.,
2003; Matsumoto et al.,
2006; Wood and Partridge,
1993). Changes in expression levels of opsin subtypes have been
associated with ontogenetic changes and metamorphic transitions, some of which
have been induced artificially with hormones or the light environment
(Beatty, 1975;
Carlisle and Denton, 1959;
Fuller et al., 2005;
Hope et al., 1998;
Mader and Cameron, 2004;
Shand et al., 2008;
Shand et al., 2002;
Takechi and Kawamura,
2005).
The other component of the VP, the chromophore, can also be varied in some
species. Many freshwater and euryhaline fishes have the ability to change
which chromophore is incorporated into their VPs, shifting between retinal
(aldehyde of vitamin A1) and 3,4-dehydroretinal (aldehyde of
vitamin A2), or using mixtures of both
(Beatty, 1984). The wavelength
of maximum absorbance (max) of a VP based on vitamin
A2 is long-wavelength shifted relative to the same opsin combined
with vitamin A1. The long-wavelength shifted vitamin
A2-based VPs are also less thermally stable than vitamin
A1-based VPs, which could have implications for species that
inhabit temperate waters where ambient temperatures vary seasonally.
Pacific salmonids are anadromous fishes restricted to temperate climates
that are equipped with a remarkably dynamic visual system that varies
temporally at different time scales throughout life history
(Allison et al., 2006a;
Allison et al., 2003;
Beatty, 1966;
Browman and Hawryshyn, 1994;
Hawryshyn et al., 1989;
Temple et al., 2006), making
this group ideal for investigating adaptive changes in visual pigment
composition.
Pacific salmon start life in freshwater as alevin. They become parr once
their yolk sac is absorbed. They may spend anywhere from a few days to a few
years in fresh water (depending on species) before migrating to sea. A
metamorphic event called smoltification precedes seaward migration, after
which they are referred to as smolts. Following a period of rapid growth at
sea, the length of which differs among species, they return to their natal
streams to spawn and die (Groot and
Margolis, 1991). During smoltification, they lose most of their
ultraviolet-sensitive (UVS) cones through programmed cell death
(Allison et al., 2006a). On
their return migration back to fresh water, some of these UVS cones are
regenerated (Allison et al.,
2006a; Beaudet et al.,
1997). It has been proposed that the VP vitamin
A1/A2 ratio in salmon might follow a similar pattern,
changing at the time of the metamorphic–migration event, with vitamin
A2 dominating in fresh water and vitamin A1 dominating
at sea (Alexander et al., 1994;
Novales Flamarique, 2005).
However, recent observations show a seasonal pattern in vitamin
A1/A2 VP ratio in all ages of coho salmon
(Oncorhynchus kisutch) (Walbaum 1792), evidence that this ratio is
correlated with seasonal changes in environmental variables and not with the
pattern of migration (Temple et al.,
2006). With regard to the timing of changes in vitamin
A1/A2 ratio, we refer to these two models as the
migration–metamorphosis and the seasonal hypotheses.
In salmonids, thyroid hormones (THs) are responsible for many of the
structural, physiological and behavioral changes associated with
smoltification, e.g. silvering, changes in body shape, increased saltwater
tolerance, change in rheotaxis, cell proliferation in olfactory epithelium,
loss of UVS cones and changes in visual pigment gene expression
(Allison et al., 2003;
Folmar and Dickhoff, 1980;
Grau et al., 1982;
Higgs et al., 1982;
Hoar, 1988;
Lema and Nevitt, 2004;
McBride et al., 1982;
Specker et al., 2000;
Staley and Ewing, 1992;
Veldhoen et al., 2006).
Earlier research established that TH treatment increased the proportion of
vitamin A2 in the VPs of coho and other salmonids
(Beatty, 1972). However, a
recent study (Alexander et al.,
1998) suggested that the direction of shift in vitamin
A1/A2 ratio may vary with temperature. Alexander et al.
(Alexander et al., 1998) found
that coho held in warm water increased the proportion of vitamin A2
in their VPs when treated with exogenous TH, but that coho held in cold water
decreased the proportion of vitamin A2 in their VPs when treated
with exogenous TH.
In the present study, we investigated the effect of TH treatment on VP compositions in coho salmon to determine whether there is variability in the direction of vitamin A1/A2 ratio shifts at different times of year and under different environmental conditions, including warm and cold temperatures. We report that TH treatment increased the proportion of vitamin A2 under all conditions tested. We also provide evidence for a change in opsin expression in middle-wavelength-sensitive (MWS) cones.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Coho were provided by two local hatcheries (Robertson Creek hatchery, Department of Fisheries and Oceans, Canada, Port Alberni, British Columbia and Target Marine, commercial hatchery, Sechelt, British Columbia). Both facilities rear coho from eggs to smolts, under natural environmental conditions, in outdoor ponds and tanks. Fish for use in these experiments were transported to the University of Victoria aquatic facilities within a few days of commencing each experiment. Care and treatment of fish was in accordance with University of Victoria's Animal Care Committee, under the auspices of Canadian Council for Animal Care.
Two different TH delivery systems were used for TH treatment: TH-treated
food and an exogenous TH bath. Both techniques are effective in stimulating
smoltification-like transitions in coho
(Alexander, 1998;
Alexander et al., 1998;
Munz and Beatty, 1965) and
vitamin A1/A2 ratio shifts in this and other species
(Allen, 1977;
Allison et al., 2004;
Beatty, 1969a;
Beatty, 1972;
Cristy, 1974;
Jacquest and Beatty, 1972).
The TH-food treatment was used in Experiments I and II to deliver TH to 150
coho housed in a 750 l cylindrical fiberglass tank with flow-through water
replacement. However, it was not possible to control the dose of TH delivered
to each fish using TH-treated food. High variation in vitamin
A1/A2 ratios among the food-treated fish and incomplete
transition to vitamin A2 VP dominance (see Results) led us to use a
bath treatment for the remaining experiments in which fewer fish were used.
Although an investigation into the differences between these two treatments
might be fruitful, it was beyond the scope of this study. Our goal was to
determine the direction of shift in vitamin A1/A2 ratio
and both TH treatments were consistent in this regard.
For Experiments I and II, fish were sampled weekly to track temporal
changes in vitamin A1/A2 ratio. TH-treated fish were fed
commercial salmon pellets sprayed with ethanol containing dissolved
L-thyroxine and 3,5,3'-triiodo-L-thyronine (Sigma,
St Louis, MO, USA). A mixture of 120 p.p.m. by weight L-thyroxine
(T4) and 12 p.p.m. 3,5,3'-triiodo-L-thyonine
(T3) was used to approximate plasma TH levels found in salmonids
prior to smoltification. This dose stimulated smoltification-like transitions
in other Oncorhynchus spp.
(Ebbesson et al., 2000;
Plate, 2001). TH-treated fish
were fed the T3–T4 diet for 1 month, and then
given the control diet for an additional 2 weeks. The control group was fed
the same commercial salmon pellets, sprayed only with ethanol, for the entire
experiment. Both control and treatment fish were fed to satiation every other
day. Weekly, three to ten fish were sampled from both control and treatment
groups (for details, see sample sizes in results).
For Experiments III–V, T4 was dissolved in 1.5 ml of 0.1 moles l–1 NaOH and added to tank water for a final concentration of 300 µgl–1 T4. Control fish received the vehicle only (1.5 ml of 0.1 moles l–1 NaOH). Water was changed three times per week. Both control and treatment groups were fed to satiation every other day with commercial salmon pellets. Five to 10 fish were sampled from both control and treatment groups after 4–6 weeks of treatment.
Microspectrophotometry
Fish were dark adapted for at least 1 hour prior to sacrifice by an
overdose of Euganol 100 mg l–1 (ICN Biomedicals, Irvine, CA,
USA), followed by cervical transection. The right eye was enucleated and
hemisected along an anterior–posterior axis. A piece of retina 1–2
mm2 was cut out of the dorsalmost section of the dorsal hemisphere.
This retinal sample was teased apart on a glass coverslip and a drop of
minimum essential medium (Sigma, Oakville, ON, Canada; pH adjusted to
7.4–7.6) was applied to the sample. A second cover slip was placed over
the sample and sealed with paraffin. All procedures were performed under
deep-red illumination (>650 nm) or using a dissecting scope equipped with
infrared LED (800 nm) illumination and monitored with a charge-coupled device
(CCD) camera.
A CCD–microspectrophotometer (MSP), which has been described
previously (Hawryshyn et al.,
2001), was used to measure spectral absorbance of individual rod
and cone photoreceptors. The CCD–MSP device delivered a short flash
[0.05–0.5 s; duration was dependent on intensity and was set to deliver
an optimum number of photons per exposure time=total counts (500 000 counts)]
of full-spectrum light [300–800 nm; 150 W xenon light source –
intensity regulated (Oriel, Stratford, Connecticut, USA)] to the photoreceptor
outer segment. Beam size was 
2x3 µm. After passing through the
sample, the transmitted beam was directed through a spectrometer [300 nm
blazed grating (Acton Research Corporation, Acton, MA, USA)] and onto a
1340x400 pixel, Peltier cooled (–45°C), back-illuminated CCD
detector (Princeton Instruments, Roper Scientific, Trenton, NJ, USA).
Photoreceptor absorbance [log10(1/T)] was calculated by
comparing the transmitted intensity through the photoreceptor
(IM) to the transmitted intensity through an area clear of
debris adjacent to the photoreceptor (IR) thus,
T=IM/IR.
Retinal samples were examined under infrared illumination (Schott RG850
filter, Ealing Optics, London, UK) and monitored by an infrared camera
(Canadian Photonics Laboratory, Minnedosa, Manitoba, Canada). The search image
and infrared filtered beam (Schott RG850 filter) were displayed on a computer
monitor. A motorized X–Y stage (Marhauser-Wetzlar
GmbH, Germany) was used to position of the photoreceptor outer segment (OS)
relative to the measurement beam. The path of the motorized stage was recorded
to prevent repeated measurements of photoreceptor OSs. Difference spectra were
used to verify that the 
-absorption band was due to the presence of a
photolabile pigment and were calculated by subtracting the bleached absorbance
curve (full spectrum bleach 2–5 s) from the initial absorbance
curve.
Criteria for acceptance of absorbance spectra were: (1) presence of a
baseline on the long-wavelength limb
(Harosi and MacNichol, 1974);
(2) max near the expected wavelength for known
Oncorhynchus spp. photoreceptors [UVS
350–380 nm;
short-wavelength-sensitive (SWS)420–450 nm; MWS490–550 nm;
and long-wavelength-sensitive (LWS)540–630 nm; rod500–530
nm (Hawryshyn et al., 2001;
Hawryshyn and Harosi, 1994)];
(3) minimal absorbance by photoproduct; and (4) signal-to-noise ratio of the
main absorption band (-band) greater than 5:1. Determinations of
max, and percent vitamin A2 from acceptable
absorbance records were performed offline subsequent to initial sampling.
A custom-designed analysis program was used to determine
max from absorbance records using existing templates. Each
MSP record consisted of over 1000 points collected between 300 and 750 nm.
Each record was linear de-trended if necessary
(Harosi, 1987). A nine-point
adjacent averaging function was used for line smoothing, and the smoothed
curve was normalized to zero at baseline on the long-wavelength arm and to one
at the center of the -band. The fit of the normalized curve was
compared with a nonlinear least-squares routine to the upper 20% of the
weighted vitamin A1/A2 ratio averaged Govardovskii et
al. (Govardovskii et al.,
2000) template (based on the center of the -peak ±40
nm).
For some rods, we also obtained a second estimate of max
based on a template created by Munz and Beatty
(Munz and Beatty, 1965) for
coho rod pigments. Rod absorbance curves were compared (minimum variance fit)
to the Munz and Beatty (Munz and Beatty,
1965) template, which extends from the max to a
point at 20% of the maximum on the long-wavelength arm. This template
(Munz and Beatty, 1965)
assumes that max values of coho rods vary from
503–527 nm. Their model is in close agreement with Harosi's
(Harosi, 1994), which predicts
that a vitamin A1-based VP with a max of 503 nm
shifts to 529 nm if the A1-based chromophore is replaced with a
vitamin A2-based chromophore in the same opsin (see Results).
However, many of the rods we measured had max values that
exceeded 527 nm and therefore would not fit the Munz and Beatty
(Munz and Beatty, 1965)
template. In these cases, we used the estimate obtained by the fit to the
Govardovskii et al. (Govardovskii et al.,
2000) template.
Gene discovery
Coho salmon parr, obtained from Robertson Creek hatchery in 2004 and
maintained in outdoor aquatic facilities, were dark adapted for 1 hour and
then killed by immersion in 300 mg l–1 tricaine
methanesulfonate (Crescent Research Chemical, Phoenix, AZ, USA). Neural retina
was dissected free of pigmented epithelium under infrared illumination.
Immediately after dissection, total RNA was isolated from the tissue using
TRIzol reagent (Invitrogen Canada, Burlington, ON, Canada) as per the
manufacturer's recommended protocol. Retinal tissue was placed in a 1.5 ml
microcentrifuge tube containing 700 µl TRIzol and was homogenized using a
disposable Kontes Pellet Pestle with cordless motor tissue grinder (Kimble
Kontes, NJ, USA). Isolated RNA was re-suspended in 50 µl RNase-free water.
RNA concentration was determined by measuring absorbance using
spectrophotometry at a standard wavelength of 260 nm. Total cDNA was
synthesized using 1 µg of total RNA. Each RNA sample was annealed with 500
ng random hexamer oligonucleotide (Amersham Biosciences, Baie d'Urfe,
Québec, Canada) and cDNA was prepared using Superscript II RNase H
reverse transcriptase (Invitrogen) as described by the manufacturer's
protocol.
A degenerate forward primer (5'-GCTATTGAGAGGTACATNGT-3') was
designed based on an alignment of consensus RH2 opsin open reading frame (ORF)
sequences and was synthesized by Operon Biotechnologies (Huntsville, AL, USA).
A degenerate reverse primer (Johnson et
al., 1993) was also used (5'-RAANATNACNGGRTTRAA-3').
All primer pairs used in this study were diluted and combined in an equimolar
ratio to a final concentration of 10 µM. Primers were used to amplify cDNA
synthesized from 1 µg parr retinal total RNA. The 20 µl reaction
contained 20 mmol l–1 Tris-HCl, 50 mmol l–1
KCl, 1.5 mmol l–1 MgCl2, 200 µmol
l–1 dNTPs, 1 µmol l–1 of each primer, 2
µl cDNA diluted 1:20 and 1.0 U Platinum Taq DNA polymerase (Invitrogen).
The thermocycle program was 94°C for 9 min, followed by 30 cycles of
94°C for 30 s, 50°C for 1 min and 72°C for 1.5 min, and a final
extension at 72°C for 10 min. Amplicons were separated in a 1.5% agarose
gel and visualized by ethidium bromide staining. The DNA band was excised from
the gel and extracted by freeze–squeeze centrifugation
(Smith, 1980). Extracted DNA
was cloned into PCR2.1-TOPO vector using the TOPO TA Cloning Kit (Invitrogen).
Plasmid DNA was purified using QIAprep Spin Miniprep Kit (Qiagen, Mississauga,
ON, Canada) and sequenced (Centre for Biomedical Research DNA Sequencing
Facility, University of Victoria, Victoria, BC, Canada). A partial RH2 opsin
sequence was obtained using the degenerate primers that differed from the
previously reported RH2 sequence for coho
(Dann et al., 2004).
The full-length coding sequence of the alternate RH2 was isolated from control fish used in Experiment III using the BD SMART RACE cDNA Amplification Kit (BD Biosciences Clontech, Mississauga, ON, Canada) according to the manufacturer's protocol; with the exception that Platinum Taq (Invitrogen) was used in the PCR reactions. Primers used in the RACE reactions were synthesized by Invitrogen and Operon Biotechnologies, respectively, as follows: 3'-RACE primer (5'CTATGCCAGCTTTGCTGCCTGGATT-3') and 5'-RACE primer (5'-GGCAGCACAGGCCATTGCCATGAC-3'). The 5'-RACE reaction used the following thermal profile: initial denaturation at 94°C for 9 min followed by 5 cycles at 94°C for 30 s, 72°C for 3 min followed by 5 cycles at 94°C for 30 s, 70°C for 30 s, 72°C for 3 min, followed by 35 cycles at 94°C for 30 s, 62°C for 30 s and 72°C for 3 min. The 3'-RACE reaction thermal profile, was 94°C for 9 min, followed by 35 cycles of 94° for 30 s, 72°C for 90 s. Amplicons were gel purified, cloned and sequenced as described above.
Sequences obtained from 5' and 3' RACE were assembled and
compared with sequences in GenBank using Blastn
(http://www.ncbi.nlm.nih.gov/BLAST/).
Sequence alignments were performed using ClustalW
(Chenna et al., 2003).
Data analysis
Statistical analyses were performed using the mean max
value obtained for each receptor class from individual fish (see
Allison et al., 2004;
Jokela et al., 2003). This
approach is not typical of MSP studies, which classically report the mean
max for each class of receptor from all fish sampled (e.g.
Cummings and Partridge, 2001;
Harosi and Kleinschmidt, 1993;
Hawryshyn et al., 2001;
Nawrocki, 1985;
Novales Flamarique, 2005).
However, it is statistically correct to treat the fish as the sample unit,
rather than the individual photoreceptors, because photoreceptors from the
same fish lack independence (pseudoreplication). When comparisons were made
between fish for a particular receptor class, we used the mean
max of all receptors collected from each fish (fish mean
max). When comparisons were made between control and
treatment groups for a particular receptor class, we used the mean
max of all fish, i.e. the mean of the fish mean
max values for all fish in each group (group mean
max).
One-way analysis of variance was used to detect differences in means among
groups over time. Independent sample t-tests were used for
comparisons between the control and treatment groups at specific time points
(=0.05).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Experiments I and II: timeline of shift in vitamin A1/A2 ratio during TH treatment
In Experiments I and II, performed in winter and summer, respectively
(Table 1), we made weekly
comparisons of the mean max of rods from both control and
TH-treated groups. In both experiments, rod max gradually
increased in TH-treated groups relative to controls, and after 4–5 weeks
TH-treated groups had shifted to significantly (P<0.05) longer
wavelengths than controls (Table
2; Fig. 1A,B). At
the end of the treatment period, when TH-treated fish were put on the control
diet, there was a rapid decrease in max, and after 2 weeks
mean max values of TH-treated and control groups were not
significantly (P>0.4) different
(Fig. 1A,B).
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Experiments III–V
In Experiments III–V, exogenous TH significantly
(P<0.001) increased group mean max of rods, MWS
and LWS cones. For rods, the long-wavelength shift in group mean
max matched that anticipated for a shift from vitamin
A1- to A2-based VP dominance
(Table 2,
Fig. 2). The distribution of
max values from all rods from all fish sampled in
Experiments III–V extended from 500 to 540 nm
(Fig. 3A).
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max values of
TH-treated groups were shifted to significantly (P<0.001) longer
wavelengths than controls in all three experiments
(Fig. 2). Among the three
experiments, the control groups did not differ significantly (ANOVA;
F16=0.861, P=0.444) nor did the TH-treated groups (ANOVA;
F17=0.209, P=0.746). The range of max
values for LWS cones extended from 563 nm to 633 nm
(Fig. 3B).
For MWS cones, like the rods and LWS cones, the max
values of TH-treated groups were shifted to longer wavelengths than the
controls in all three experiments. However, we did not perform ANOVA tests
because we had evidence that more than one variable was changing (see below).
The group mean max values for MWS cones ranged from 501.5
to 547.7 nm (Fig. 2). The range
of max values for all individual MWS cones (from all fish,
from Experiments III–V) spanned a spectral range from below 490 nm to
above 550 nm (Fig. 3C). Both
measures of change in max suggest a shift that was greater
than predicted for a shift from vitamin A1- to A2-based
chromophores in a single opsin. There are six empirical models that predict
the change in max
(
max=A2max–A1max)
that occurs when vitamin A1 and A2 chromophores are
exchanged in a single VP opsin (Bridges,
1965; Dartnall and Lythgoe,
1965; Harosi,
1994; Parry and Bowmaker,
2000; Tsin et al.,
1981; Whitmore and Bowmaker,
1989). For vitamin A1-based VPs with
max values between 495 nm and 512 nm
(Fig. 4),
max is predicted to be between 16.6 nm
(Parry and Bowmaker, 2000) and
36.0 nm (Whitmore and Bowmaker,
1989). The max value we observed for MWS
cones was between 46.2 nm and 60 nm (13.8 nm range for
max is the difference between using the group mean
max value or the mean of all individual cones,
respectively). Regardless of how it was calculated, the magnitude of
max was greater than predicted by any of the
existing models. We therefore hypothesized that more than one subtype of the
RH2 opsin was being expressed in coho MWS cones. Given this proposed
explanation, it was not appropriate to treat all MWS cones as if originating
from a single normally distributed population. Therefore, MWS cone
max values are hereafter described by the range of
max values recorded from all individual MWS cones from each
group of fish.
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Modeling multiple opsins in MWS cones
Estimating the max of the hypothesized opsin subtypes
was complicated by the variation in max that resulted from
the variable chromophore ratio. To address this, we plotted
max values from measurements made on 100 MWS–LWS
double cones from which both OSs had been recorded
(Fig. 5). The expectation for
such a plot, for a species with only one opsin in each of its double cone OSs
and using only one chromophore type (i.e. not coho salmon), is a single
tightly clumped distribution of max values. For a species
with only one copy of each opsin but the ability to use both vitamins
A1 and A2 (as was thought to be the case for coho), the
prediction is a distribution of points tightly grouped along a straight line
that extends diagonally away from the origin
(Loew and Dartnall, 1976). Our
observation did not match either of these predictions and, instead, looked
like a diagonal line with a positive slope stretched out along the horizontal
axis (Fig. 5). This
distribution indicated the presence of more than one opsin being expressed in
MWS cone OSs.
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To estimate max values of the two hypothesized opsin
subtypes, we defined the limits of the distribution with lines that took into
account a measurement error of ±3 nm on all sides
(Fig. 5), except the lower side
(see below). The distribution of max values for LWS cones
extended from 563 to 633 nm. The distribution for MWS cones extended from 495
to 548 nm. To calculate the max values of the corresponding
vitamin A1- or A2-based VP pairs, we assigned the lower
limit of the max values as the max for
the vitamin A1-based VP and the upper limit as the vitamin
A2-based VP. These values were then used in equations provided in
the six published models predicting max
(Bridges, 1965;
Dartnall and Lythgoe, 1965;
Harosi, 1994;
Parry and Bowmaker, 2000;
Tsin et al., 1981;
Whitmore and Bowmaker, 1989)
to estimate the max of predicted VP pair. As a conservative
measure, to reduce the probability of Type I error, we compared our observed
data set with the model that predicted the largest
max for the given vitamin
A1–A2 VP pair [Harosi's
(Harosi, 1994) model for the
long-wavelength range and Whitmore and Bowmaker's
(Whitmore and Bowmaker, 1989)
for the middle-wavelength range].
The LWS cone max distribution was explained by a single
LWS opsin combining with vitamins A1 and A2 to give a
range of 5631–6332 nm (subscripts denote vitamins
A1 and A2 chromophore types, respectively). The most
parsimonious model to account for the observed range in MWS cones was to
assign the longest value (548 nm) as the vitamin A2 state of one VP
pair and the shortest value (495 nm) as the vitamin A1 state of a
second VP pair. We proposed that one VP pair had a range of
4951–5232 nm and the other VP pair had a range of
5121–5482 nm.
Molecular evidence for two RH2 opsin subtypes
To test the hypothesis that coho express a second RH2 opsin subtype,
retinal material was collected from fish that showed a large range in MWS cone
max values. Two subtypes of the RH2 opsin were isolated,
cloned and sequenced. One subtype had been previously identified in coho [RH2
(Dann et al., 2004)], here
renamed RH2A, and the second was a novel RH2 sequence that we have named RH2B
(GenBank Accession Number DQ309027) in accordance with nomenclature recently
used for other fish opsin subtypes
(Carleton and Kocher, 2001;
Collin et al., 2003;
Matsumoto et al., 2006).
The possession of several amino acids that are conserved among vertebrate
opsins suggests that RH2B is a functional opsin. The predicted RH2B amino acid
sequence has a lysine at position 296 that forms a Schiff's base linkage with
the chromophore (Wang et al.,
1980). RH2B has glutamic acid at position 113, which is the
counter ion of the protonated Schiff's base
(Sakmar et al., 1989;
Zhukovsky and Oprian, 1989),
and cysteine residues at positions 110 and 187, which form a disulphide bond
within the opsin (Karnik et al.,
1988). RH2B also has three amino acids, S240, T243 and V250, which
are located in cytoplasmic loop 3 and are conserved in all opsins
(Archer, 1995).
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max of these pigments (see Discussion).
Summary of results
The main findings of these experiments were: (1) exogenous TH induced
smoltification-like transitions in pre-smolt coho under all environmental
conditions tested and throughout the year; (2) exogenous TH resulted in a
long-wavelength shift in rod max in all five experiments;
(3) the observed range of group mean max values for rods
(503–533 nm) was consistent with a shift in vitamin
A1/A2 ratio; (4) the range of max
values observed for MWS cones extended from 495 to 548 nm, which was greater
than predicted for a shift in vitamin A1/A2 ratio within
a single opsin; and (5) a second RH2 opsin subtype was isolated, cloned and
sequenced.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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max of all photoreceptors
regardless of differences in age, time of year, rearing conditions or TH
delivery method. In rods, the 30 nm increase in group mean
max was consistent with a change in vitamin
A1/A2 VP ratio based on predicted
max values
(Bridges, 1965;
Dartnall and Lythgoe, 1965;
Harosi, 1994;
Parry and Bowmaker, 2000;
Tsin et al., 1981;
Whitmore and Bowmaker, 1989).
This TH-induced increase in vitamin A2 is consistent with nearly
all previous studies with teleosts
(Alexander et al., 1998;
Allen, 1971;
Allen, 1977;
Allison et al., 2004;
Beatty, 1969a;
Cristy, 1974;
Jacquest and Beatty, 1972;
McFarland and Allen, 1977;
Munz and Swanson, 1965;
Tsin and Beatty, 1979), except
one trial in a study by Alexander et al.
(Alexander et al., 1998), which
showed a decrease in vitamin A2 in coho reared at cold temperatures
(5°C). Further investigation is required to understand the factors that
account for the difference between our results in cold water (3–5°C)
and those of Alexander et al. (Alexander et
al., 1998).
The max values recorded from individual rods, rather
than group mean values, had a range that was greater than the
max models predicted, and the mean
max of rods from the TH-bath treated fish was 532.7 nm,
which is long-wavelength shifted by nearly 5 nm relative to previous reports
for coho salmon (Alexander,
1998; Alexander et al.,
1994; Beatty,
1972; Munz and Beatty,
1965; Temple et al.,
2006). One explanation is that our TH-bath treatment may have
resulted in a complete transition to vitamin A2-based VPs, whereas
previous studies used fish that may have had intermediary vitamin
A1/A2 ratios owing to the source of fish or treatments
given [e.g. wild versus untreated fish
(Alexander et al., 1994;
Temple et al., 2006), TH in
diet (Alexander et al., 1998)
(present study), or intraperitoneal injections of TH for less than 14 days
(Beatty, 1972)]. The large
shifts in max, resulting from TH treatment may rarely occur
naturally, but they demonstrate the extent of adaptability of this
species.
Alternatively, it is possible that a second opsin subtype is expressed in
coho rods. European eels (Anguilla anguilla L.) express two RH1 opsin
subtypes. Under natural conditions, the European eel alters expression of its
RH1 opsin subtypes upon migrating from fresh water to the sea
(Carlisle and Denton, 1959),
and they have been induced to shift between the two subtypes using exogenous
hormone treatment (Hope et al.,
1998; Wood and Partridge,
1993). Recent evidence suggests that rainbow trout (O.
mykiss) could also have two RH1 opsin genes
(Allison et al., 2006b). The
expression of these two genes was shown to vary between TH-treated and control
fish, as proposed here for the RH2 opsin subtypes. It is possible that the
wide range of values observed for rods was the result of a TH-induced shift to
a second RH1 opsin subtype in coho.
LWS cone max range
In our plot of LWS verses MWS cone max values, we
observed three outliers below the lower horizontal line at 563 nm, which
delineated the vitamin A1 state of the proposed LWS opsin
(Fig. 5). The data points came
from three separate control fish. We are collecting measurements from
additional fish as part of a subsequent study to define more accurately the
lower limit of max values for LWS cones in coho salmon.
Again, we would like to suggest this is preliminary evidence for the presence
of multiple subtypes of the LWS opsin.
Two RH2 opsin subtypes in coho MWS cones
MSP and molecular approaches have provided independent evidence for the
presence of two RH2 opsin subtypes in coho salmon. The max
values recorded from MWS cones ranged from 495 nm to 548 nm
(max=53 nm). This observation argues strongly for
two opsin subtypes, especially in the context of several models predicting a
max no greater than 36 nm
(Bridges, 1965;
Dartnall and Lythgoe, 1965;
Harosi, 1994;
Parry and Bowmaker, 2000;
Tsin et al., 1981;
Whitmore and Bowmaker, 1989).
Our molecular analysis led to the isolation and sequencing of a novel subtype
of the RH2 opsin gene, thus confirming our hypothesis. When compared with the
existing sequence [RH2A (Dann et al.,
2004)], there were 48 amino acid differences
(Fig. 6). Key among these is
likely to be the substitution of glutamate for glutamine at position 123,
which is analogous to 122 in bovine RH1. This particular site plays an
important role in spectral tuning of both RH1 and RH2 opsins
(Yokoyama et al., 1999). The
E122Q substitution results in a short-wavelength shift in bovine RH1 by
20–25 nm (Sakmar et al.,
1989). In zebrafish, three out of the four RH2 opsin subtypes have
glutamate at position 122 and all three absorb maximally at shorter
wavelengths (17–38 nm) than the fourth, which has glutamine at position
122 (Chinen et al., 2003;
Chinen et al., 2005). Based on
our estimates from Fig. 5, the
predicted values for the RH2A and RH2B opsin subtypes, when combined with
vitamin A1, were 5121 nm and 4951 nm,
respectively. This observed shift in max was within the
range previously reported for other opsins differing by an E122Q substitution.
Based on its sequence and on our MSP results, RH2B was short-wavelength
shifted by 17 nm relative to RH2A.
The magnitude of shift in max between control and
TH-treated groups suggested that TH played a role in regulating expression
levels of RH2A and RH2B opsin subtypes. This is consistent with the function
of TH as a signaling mechanism in vertebrate metamorphosis
(Power et al., 2001), and in
retinal development and opsin expression
(Allison et al., 2003;
Browman and Hawryshyn, 1992;
Harpavat and Cepko, 2003;
Roberts et al., 2006). Current
efforts in our laboratory are aimed at determining the spatiotemporal
expression patterns of RH2A and B opsins in coho and other Pacific
salmonids.
The ecological significance of the second RH2 opsin subtype was not
immediately evident. The max of MWS cones in TH-treated
fish were long-wavelength shifted relative to control fish, suggesting that
the natural state for post smoltification coho was to express the
long-wavelength shifted RH2A opsin. This would seem counterintuitive as after
smoltification, coho migrate to sea where the spectral distribution is
short-wavelength shifted relative to most freshwater habitats
(Tyler and Smith, 1970).
A similar shift in max of MWS cones was reported to
occur naturally in coho by Novales Flamarique
(Novales Flamarique, 2005). He
described the change in MWS cone max as being a
`compensatory' shift in response to the simultaneous loss of UVS cones from
the retina. We suggest that MWS cones are shifted to longer wavelengths so
that they are offset from the main spectral distribution of light along the
sidewelling line of sight. Several marine fish have been shown to employ this
tactic to enhance the detection of bright reflective targets against the
nearly monochromatic blue–green background
(McFarland and Munz, 1975).
When coho move from fresh water to sea they shift their diet from
predominantly terrestrial and aquatic insects to small fish and crustaceans.
Crypsis in freshwater streams is accomplished by earthy and dark coloration
patterns that match the substrate, therefore prey detection would be optimized
by having VPs matched to the spectral background. In the open ocean, crypsis
is accomplished by being transparent, or silvery, to reflect the monochromatic
background light (Denton and Nicol,
1965; Johnsen,
2002; McFall-Ngai,
1990). The long-wavelength shift in MWS cone
max would offset the VP improving the detection of brightly
colored prey. The change in MWS cone max might be equally
important for conspecific recognition. Coho are territorial while in
freshwater streams but join schools when they enter the estuaries, and they
alter their appearance at smoltification by changing their dark reddish-brown
parr marks and dorsal pigmentation to silvery sides and blue–green
dorsal pigmentation (Groot and Margolis,
1991).
Migration–metamorphosis or seasonal vitamin A1/A2 ratio shift
Our observation, of an increase in vitamin A2 with the
application of TH lends support to the seasonal hypothesis for explaining the
timing of shifts in A1/A2 ratio. Given that metamorphic
transitions are driven by TH signaling mechanisms in vertebrates
(Mader and Cameron, 2004;
Power et al., 2001), and that
TH induces smoltification-like transitions in salmon (see Introduction), then
under the migration–metamorphosis hypothesis, it would be expected that
TH induce a decrease in A2 as naturally occurs when salmon undergo
smoltification prior to seaward migration. In fact the opposite was observed.
The max of rods increased in a manner consistent with an
increase in vitamin A2 under all conditions tested, leading us to
conclude that the vitamin A1/A2 ratio is independent of
smoltification in coho salmon. These findings support our previous
observations (Temple et al.,
2006) that the A1/A2 ratio in coho salmon is
linked to seasonal environmental changes, a pattern also observed in other
teleosts (Allen et al., 1982;
Beatty, 1969b;
Dartnall et al., 1961;
Ueno et al., 2005), amphibians
(Makino et al., 1983) and
invertebrates (Suzuki et al.,
1984).
The selective advantage of shifting from vitamin A2 in winter to
vitamin A1 in summer could be that it improves the signal-to-noise
ratio in the face of seasonal variation in temperature and light conditions.
Vitamin A1-based VPs are more thermally stable than are vitamin
A2-based VPs (Ala-Laurila et
al., 2003; Ala-Laurila et al.,
2004; Barlow,
1957). And because photoreceptors are unable to distinguish
between photo- and thermal-isomerization events
(Barlow, 1957) vitamin
A1-based VPs will provide a higher signal-to-noise ratio
(Aho et al., 1988;
Barlow, 1988). The eyes of
exothermic organisms such as fish, amphibians and invertebrates are subject to
environmental changes and as temperature increases, the signal-to-noise ratio
worsens (Baylor et al., 1980).
The possible advantages of long-wavelength-shifted vitamin A2-based
VPs must be countered by the poorer signal-to-noise ratio at higher
temperatures (Allen and McFarland,
1973). We interpret the variable vitamin
A1/A2 ratio in coho as a trade-off between increasing
spectral breadth of sensitivity and minimizing noise when temperatures rise
(Temple et al., 2006).
In summary, exogenous TH produced long-wavelength shifts in photoreceptor
max that were explicable by changes in vitamin
A1/A2 VP chromophore ratio combined with changes in
opsin subtype expression. In addition to expressing representatives of all
five vertebrate opsin classes, coho were found to express at least two
subtypes of RH2 opsin. Our MSP evidence also indicates the possibility of two
subtypes of the RH1 and LWS opsin genes. The potential to vary spectral
sensitivity, through variable opsin expression together with alterations in
the vitamin A1/A2 VP ratio, provides coho with a dynamic
visual system that operates over spatially and temporally diverse spectral
environments encountered throughout their complex life history.
LIST OF SYMBOLS AND ABBREVIATIONS
max
RH1, RH2, SWS1, SWS2, MWS, LWS, UVS, RH2A, RH2B are all short forms for opsins and cone types as described in the text
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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  S. E. Temple, K. M. Veldhoen, J. T. Phelan, N. J. Veldhoen, and C. W. Hawryshyn Ontogenetic changes in photoreceptor opsin gene expression in coho salmon (Oncorhynchus kisutch, Walbaum) J. Exp. Biol., December 15, 2008; 211(24): 3879 - 3888. [Abstract] [Full Text] [PDF]
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