Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development
Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan
* Author for correspondence (e-mail: kawamura{at}k.u-tokyo.ac.jp)
Accepted 8 February 2005
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Summary |
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Key words: visual pigment, opsin, zebrafish, retina, differential expression
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Introduction |
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The so-called red and green opsins of humans belong to the M/LWS type and
were created by gene duplication of an ancestral single-copy M/LWS opsin gene
during primate evolution and, hence, are subtypes of M/LWS opsins. Besides the
M/LWS opsins in primates, occurrence of opsin subtypes has only been reported
in fish. There are the M/LWS opsins of Mexican cavefish (R007, G101 and G103;
Yokoyama and Yokoyama, 1990),
RH2 opsins of goldfish (GFgr-1 and GFgr-2;
Johnson et al., 1993
), SWS2
opsins of cichlid (SWS2-A and SWS2-B;
Carleton and Kocher, 2001
) and
RH1 opsins of eels (fresh-water and deep-sea types;
Archer et al., 1995
;
Zhang et al., 2000
).
We recently screened a zebrafish genomic library for subtype repertoires in
all five types of the visual opsins
(Hamaoka et al., 2002;
Chinen et al., 2003
). Zebrafish
were found to possess two subtypes of M/LWS opsin genes, LWS-1 and
LWS-2, and four RH2 subtype genes, RH2-1, RH2-2, RH2-3 and
RH2-4, in addition to a single-copy of RH1, SWS1 and SWS2 opsin genes
(Chinen et al., 2003
). The two
M/LWS opsin genes are arrayed in tandem with a 1.8 kb interval, 2.5 kb
downstream from the SWS2 opsin gene in the chromosomal linkage group (LG) 11
(see also GenBank accession no. AL844847 for a zebrafish genome sequence
containing the three genes under symbol names opn1sw2, opn1lw1 and
opn1lw2 for SWS2, LWS-1 and LWS-2, respectively).
The four RH2 opsin genes are also arranged in tandem in approximately a 25 kb
genomic region in the LG 6 (see GenBank AL732567 for a genome sequence
containing the four genes under symbol names opn1mw1, opn1mw2,
opn1mw3 and opn1mw4 for RH2-1, RH2-2, RH2-3 and
RH2-4, respectively). Importantly, absorption spectra represented
with the wavelength of peak absorbance (
max), differ markedly between
the two M/LWS pigments reconstituted with the A1 chromophore in vitro
at 558 nm (LWS-1) and 548 nm (LWS-2). The four
A1-reconstituted RH2 pigments are at wavelengths 467 nm (RH2-1), 476
nm (RH2-2), 488 nm (RH2-3) and 505 nm (RH2-4)
(Chinen et al., 2003
). These
subtype genes are all expressed in the adult zebrafish retina with
LWS-1 and RH2-2 having the highest expression level within
each type (Chinen et al.,
2003
).
Occurrence of opsin subtypes in fish may reflect the diversity of aquatic
light environments. However, documented variations of spectral sensitivities
of visual pigments among fish species are mostly attributed to chromophore
type A1 or A2 (Bowmaker, 1995),
evolutionary changes of opsin amino acid sequences
(Yokoyama, 2000
), opsin types
expressed in the retina (Carleton and
Kocher, 2001
), or developmental changes of expressed opsin types
in a photoreceptor cell (Cheng and Novales
Flamarique, 2004
). Only two cases of differential usage of opsin
subtypes have been reported; RH1 opsins of eels at different ontogenic stages
(fresh-water and deep-sea types; Archer et
al., 1995
; Zhang et al.,
2000
) and SWS2 opsins of cichlids where different species
inhabiting different niches expressed different subtypes (SWS2-A and SWS2-B;
Carleton and Kocher, 2001
).
Little is known how opsin subtypes are distributed phylogenetically and
ecologically among fish species and how differently they are expressed in the
retina spatially and temporally in a given species.
In this study we examined expression of subtype opsin genes of zebrafish,
the only fish species whose complete repertoires of visual opsin genes have
been isolated and spectrally characterized
(Chinen et al., 2003). We have
shown by in situ hybridization (ISH) that the M/LWS and RH2 opsin
genes are expressed differently among subtypes in spatial distribution in the
retina during development of zebrafish.
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Materials and methods |
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Similarly, RNA probes for the full-length CDR were prepared for
LWS-2 (1071 nucleotides [nt]; GenBank AB087804), RH2-1 (1050
nt; GenBank AB087805), RH2-4 (1050 nt; GenBank AB087808),
SWS1 (1011 nt; GenBank AB087810), SWS2 (1065 nt; GenBank
AB087809) and RH1 (1065 nt; GenBank AB087811) from their cDNA clones
previously isolated, either in pBluscript II (SK) (Stratagene, La
Jolla, CA, USA) or pGEM-T easy vector
(Chinen et al., 2003).
In situ hybridization (ISH)
Zebrafish (Danio rerio) were maintained at 28.5°C in 14 h:10 h
light:dark cycle by following a standard procedure
(Westerfield, 1995). Embryos
[defined here as fish up to 3 days post fertilization (dpf)] of zebrafish WIK
strain were raised in 0.003% 1-phenyl-2-thiourea after 12 h pf (hpf) to
disrupt pigment formation and were subjected to whole-mount ISH as previously
described (Hamaoka et al.,
2002
). For ISH of larvae (defined as 3 days to 1 month pf) and
juveniles (defined as 12 months pf), we used an albino strain, B4, to
facilitate observation of the photoreceptor layer, which is masked in
non-albino strains by the dark retinal pigment epithelium. The albino mutation
has been shown not to affect opsin genes and pattern formation of retinal
cells (Nawrocki et al., 1985
;
Ren et al., 2002
). Whole
bodies of larvae and dissected heads of juveniles were subjected to ISH. For
adults (defined as after 2 months pf; WIK strain), light-adapted eyes were
enucleated and lenses were removed. The samples were soaked in fixer (4%
paraformaldehyde, 0.1 mol l1 phosphate-buffer) overnight at
4°C. For some samples, the fixer was directly injected into the inside of
the eyecup, which is filled with viscoid fluid, immediately after enucleation
of the eyes and then soaked in the fixer overnight at 4°C to reduce RNA
degradation during fixation. Cryosections of retinas were prepared and
hybridized to the RNA probes as previously described
(Hamaoka et al., 2002
). In this
study, to compare expression patterns among different subtype opsins, adjacent
sections from the same eyes were hybridized with different probes so that
entire expression patterns of opsin subtypes in the retina could be
reconstructed. After hybridization, samples were washed at 65°C twice in
50% formamide, 2 x SSC (1 0.15 mol l1 NaCl, 0.015 mol
l1 sodium citrate, pH 7.6) for 30 min each, once in 2
x SSC for 10 min and twice in 0.5 x SSC for 20 min each. The
samples were then rinsed twice in MABT (0.1 mol l1 maleic
acid, 0.15 mol l1 NaCl, 0.1% Triton-X, pH 7.5) at room
temperature, soaked once in 2% blocking reagent (Roche) in MABT for 30 min,
incubated with anti-DIG antibody (1:2000 dilution) in the blocking solution
for 2 hours, and washed six times in MABT for 10 min each.
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Results |
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When using the RH2-1 CDR probe, which detects both RH2-1
and RH2-2 transcripts, the first hybridization signal was detected at
45 hpf in a ventral patch, which was in the nasal side of choroid fissure
(Fig. 1A). The signal spread to
the nasal and central retina (Fig.
1B), then to ventrotemporal retina
(Fig. 1C), and finally to the
dorsal retina (Fig. 1D), being
largely concordant with previously reported progression patterns of the red
and blue opsin gene expression (Raymond et
al., 1995). We then used RH2-1 and RH2-2
3'-UTR probes (38% identity between the two probes) to distinguish
expressions of the two genes. Identical results were obtained using the
RH2-1 3'-UTR probe, but no reliable signal was detected using
the RH2-2 3'-UTR probe in embryos examined up to 72 hpf,
indicating that the hybridization pattern using the RH2-1 CDR probe
represented the expression pattern of RH2-1, and that RH2-2
is not expressed in the embryonic stage at a detectable level.
|
When we used the RH2-4 CDR probe, which detects both RH2-3 and RH2-4, the first signal appeared weakly at 72 hpf in the most marginal side of nasal retina in a broad area (Fig. 1E). This pattern of expression is different to those in other opsins where it is initiated in a ventral spot, as in RH2-1 (see Fig. 1A). However, no signal was detected using either RH2-3 or RH2-4 3'-UTR probe (70% identity between the two) and we could not distinguish which subtype was expressed between RH2-3 and RH2-4. This is likely due to the shortness of the 3'-UTR probes compared with the CDR probe (see Materials and methods for their lengths).
RH2 opsin expression in larval and juvenile zebrafish retina
Following RH2-1, expression of RH2-2 was observed
throughout the retina by 7 dpf. However, at 16 dpf, expression of
RH2-1 disappeared in the marginal area of retina
(Fig. 2A, double arrows), in
contrast, RH2-2 expression disappeared in the central retina in many
photoreceptor cells (Fig. 2B,
double arrow). This tendency was more obvious at 1 month pf, where expression
of RH2-1 was confined to the central area
(Fig. 2D) and that of
RH2-2 in the area surrounding it
(Fig. 2E). In addition,
RH2-2 expression at this stage disappeared in the ventral margin of
the retina (Fig. 2E, area below
the triple stars), and the expression of RH2-3/RH2-4 filled
the space (Fig. 2F), which was
detected by the RH2-4 CDR probe (but not by either the RH2-3
or RH2-4 3'-UTR probe as in
Fig. 1E). At 16 days pf, the
RH2-4 CDR probe detected a few signals in this area
(Fig. 2C, arrows), which were
again not detectable by the 3'-UTR probes for RH2-3 and
RH2-4. It was noted that at 1 month pf, expression areas of
RH2-1 and RH2-2 overlapped at the boundaries (single and
double stars in Fig. 2D and E)
and so were those of RH2-2 and RH2-3/RH2-4 (triple
stars in Fig. 2E and F).
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RH2 opsin expression in adult zebrafish retina
In adults (2 years old), expression pattern of RH2-1 was
consistent with that at 1 month pf, where it covered the central to dorsal
area of the retina (Fig. 2G).
By contrast, RH2-2 expression changed dramatically; the central area
of expression in the retina, which disappeared in the larval to juvenile
stages (Fig. 2B,E), was
restored (Fig. 2H) so that the
RH2-2 expression covered a larger central to dorsal area than the
RH2-1 area. The restoration of the central expression of
RH2-2 occurred between 12 months pf. The hybridization signal
of RH2-2 was much stronger than that of RH2-1, which was
consistent with our previous observation in real-time RT-PCR, in that the
expression level of RH2-2 in adult retina is significantly higher
than the other RH2 subtype genes (Chinen et
al., 2003).
In adults we were able to detect expression of RH2-3 and RH2-4 separately using the 3'-UTR probes. RH2-4 was expressed in the ventral side of retina (Fig. 2I, area below the arrow head) and at the ciliary marginal zone (CMZ) (Fig. 2I, arrow). RH2-3 expression was confined to a narrow zone in the centro-ventral area and dorsal CMZ (Fig. 3A, double arrows). When expression areas of RH2-3 and RH2-4 were compared in adjacent sections prepared from the same eyes, the RH2-3 and RH2-4 zones did not appear to overlap (Fig. 3B and C). In addition, in the centro-ventral area the edge of the RH2-2 zone (Fig. 2H, arrowhead) and that of RH2-4 zone (Fig. 2I, arrowhead) also appeared not to overlap.
|
A previous immunohistochemical study using an antibody against a zebrafish
green opsin (zfgr1, corresponding to RH2-1) showed that green opsin
is produced only in short double cones (SDC) in adult zebrafish retina
(Robinson et al., 1993;
Vihtelic et al., 1999
). An ISH
study using goldfish green opsin cRNA probe, which is more closely related to
RH2-3/RH2-4 than to RH2-1/RH2-2
(Chinen et al., 2003
), also
localized the hybridization signal to SDC in adult zebrafish retina
(Raymond et al., 1993
;
Robinson et al., 1993
). Our
ISH to tangential sections of adult retina confirmed that RH2-1,
RH2-2 and RH2-4 were expressed only in SDC in the square mosaic
arrangement of cones (Robinson et al.,
1993
) using RH2-1 CDR and RH2-4 3'-UTR
probes (data not shown). The RH2-3-expressing zone was too narrow for
us to determine reliably its cell type in the cone mosaic. However, it is most
likely that all RH2 subtype genes are expressed in SDC.
LWS opsin expression in zebrafish retina
Transcripts of the two M/LWS (red) opsin genes, highly homologous in CDR
(93% identity), were distinguished using the 3'-UTR probes (48% identity
between the two genes). Expression of LWS-2 was first observed at 40
hpf as a ventral patch in the retina. It then spread throughout the retina in
the same spatial pattern as shown for RH2-1
(Fig. 1AD). In contrast,
initial expression of LWS-1 was observed in 3.55.5 dpf in a
broad area in the marginal side of the ventral retina
(Fig. 1F). These results
indicate that the red opsin expression reported in previous studies
(Raymond et al., 1995;
Schmitt et al., 1999
) is that
of LWS-2 but not of LWS-1 (LWS-1 was originally
known as a sole cDNA species of zebrafish red opsin,
Schmitt et al., 1999
;
Vihtelic et al., 1999
;
Chinen et al., 2003
).
At 1 week pf, while expression of LWS-1 was confined to the ventral side of the retina, the expression of LWS-2 was present in the entire retina. At 1 month pf, ISH in transverse retinal sections showed that expression of LWS-2 disappeared in the ventral side (Fig. 4B, area below the star) where complementarily LWS-1 expression was observed (Fig. 4A). It was noted that expression areas of the two genes overlapped at the boundary (Fig. 4A,B, stars). Expression of LWS-1 was also observed sparsely in photoreceptor cells in the central to dorsal retina (Fig. 4A, arrows).
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In sexually mature adults (2 years old), expression of LWS-1 was
observed not only in the ventral area but also in the dorsal periphery
(Fig. 4C, solid double arrows).
In addition, the number of cone cells expressing LWS-1 appeared to
increase in the central and dorsal areas
(Fig. 4C, dotted double
arrows). Conversely, LWS-2 was expressed in the central to dorsal
retina but was not in the dorsal peripheral region
(Fig. 4D, bracket). The
expression profiles of the two genes are complementary in the retina, although
cells at the boundary of the two fields and those expressing LWS-1 in
the central LWS-2 zone appeared to express both gene subtypes. It was
noted that the hybridization signal of LWS-1 was stronger than that
of LWS-2 using the same amount of probe, which is consistent with our
previous observation by real-time RT-PCR, that the LWS-1 transcript
is more abundant than that of LWS-2 in the adult retina
(Chinen et al., 2003). Previous
immunohistochemical and ISH studies showed that red opsin is produced only in
long double cones (LDC) in adult zebrafish retina
(Raymond et al., 1993
;
Robinson et al., 1993
;
Vihtelic et al., 1999
). Our
ISH to tangential sections of retina confirmed that both LWS-1 and
LWS-2 genes are expressed in LDC (data not shown).
Sequence of expression among opsin types in embryonic zebrafish retina
We also examined the onset times of other opsin types SWS1, SWS2 and RH1,
together with M/LWS and RH2 opsins to re-evaluate relative onset timing among
the five types of opsins by using their full-length CDR probes. LWS-2
and RH2-1 were used to represent M/LWS and RH2 types, respectively,
because they are the first subtypes expressed in their opsin types.
Whole-mount ISH was performed on embryos sampled at 40, 45, 50, 55, 60 and 72
hpf andexpression patterns of the opsin genes were assigned to appropriate
stages according to Raymond et al.
(1995), Hamaoka et al.
(2002
) and Takechi et al.
(2003
)
(Fig. 5). RH1 and M/LWS were
the first opsins showing expression in the retina (at 40 hpf), consistent with
previous studies (Raymond et al.,
1995
; Schmitt et al.,
1999
), and were followed by SWS1 and RH2 (at 45 hpf) and then SWS2
(at 50 hpf), which differed from the order suggested in a previous study, i.e.
green, blue and ultraviolet (Schmitt et
al., 1999
). We noticed that the DNA sequence assigned to the
zebrafish blue opsin gene (GenBank AF104903) in Schmitt et al.
(1999
) was in fact that of
SWS1 (i.e. ultraviolet) but not of SWS2 opsin genes, which could have
introduced an error in the evaluation of the expression order among the opsin
genes.
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Onset times of the five opsin types in this study (4050 hpf) were
overall earlier than those reported in the previous studies (5055 hpf)
(Raymond et al., 1995;
Schmitt et al., 1999
). The
early onset times may be partly due to the fact that Schmitt et al.
(1999
) selected only embryos
that had achieved certain developmental characteristics at certain time points
to minimize individual variation whereas we did not do any selection (see also
Takechi et al., 2003
).
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Discussion |
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In early development of zebrafish, expression of LWS-2, the
shorter-wavelength subtype of M/LWS opsins (max at 548 nm), precedes
expression of LWS-1, the longer-wavelength-sensitive subtype (558
nm), and is distributed more widely in the retina than LWS-1
expression (Fig. 6).
Conversely, in the adult retina expression level of LWS-2 is lower
than that of LWS-1 (Chinen et al.,
2003
), indicating an overall spectral shift of M/LWS opsin type
from short to long wavelength direction throughout development. This is
consistent with an earlier observation by microspectrophotometry (MSP) that
max of a class of double cone shifts from
540 nm in early larvae
(68 dpf) to
560 nm in late larvae (1117 dpf) and adults
(12 years old) (Nawrocki et al.,
1985
).
Among the four RH2 opsin genes, the shortest-wavelength subtype
RH2-1 (467 nm) is first expressed throughout the retina by 3 dpf
(Fig. 7). Subsequently,
expression of RH2-2 (476 nm) spreads throughout the retina by
1
week pf and passes through a period of disappearance in the central retina at
around two weeks to 1 month pf; its expression level becomes highest among the
four subtypes in the adult retina (Chinen
et al., 2003
). However, unlike M/LWS opsins, longer-wavelength
subtypes RH2-3 (488 nm) and RH2-4 (505 nm) remain expressed
at the periphery and at a low level (Chinen
et al., 2003
) throughout development. Although there is no MSP
data before 68 dpf forzebrafish, MSP for middle-wavelength-sensitive
cones after this period shows that their mean
max values are at around
475480 nm, with a relatively lower one (475 nm) found at 1117
dpf (Nawrocki et al., 1985
),
which appears consistent with our results.
In adult retina, the shorter-wavelength-sensitive subtypes LWS-2, RH2-1 and RH2-2 are expressed in the central to dorsal area and the longer ones LWS-1, RH2-3 and RH2-4 are in the periphery, especially in the ventral area (Figs 6 and 7). RH2-3 is expressed circularly surrounding the RH2-2 zone and RH2-4 is expressed outside of the `RH2-3 ring' with a broader area in the ventral side of the retina.
Ontogenic and regional differentiations of photoreceptors in their spectral
sensitivity are classical and well documented phenomena in many vertebrates
including fish and mammals (Levine and
MacNichol, 1982; Ahnelt and
Kolb, 2000
). The phenomena have been ascribed to differential
usage of opsin types or chromophore types. The loss of UV cones and the change
to blue cones in salmonid fish is a well recognized example
(Cheng and Novales Flamarique,
2004
). However, in zebrafish the single-copy SWS1, SWS2 and RH1
opsins are expressed uniformly in the retina throughout development
(Vihtelic et al., 1999
;
Hamaoka et al., 2002
;
Takechi et al., 2003
) and only
A1 chromophore is used throughout development under natural conditions
(Nawrocki et al., 1985
;
Saszik and Bilotta, 1999
).
Besides primate M/LWS opsin genes, occurrence of opsin subtypes is
characteristic of fish, and the resulting variations of opsin repertoire among
species should be intricately involved in the evolutionary adaptations of fish
to diverse aquatic photo-environments. To date, however, the only known
example of differential usage of opsin subtypes in a given fish species has
been the ontogenic shift of rod opsin expression between fresh-water and
deep-sea subtypes in eels (Archer et al.,
1995
; Zhang et al.,
2000
).
The present study provides the first evidence that subtype differentiation of cone opsins in fish contributes not only to temporal but also to regional differentiation of the retina with distinct spectral sensitivities. Spectral difference between opsin subtypes is generally smaller than that between different cone opsin types. Subtype differentiation of opsins in absorption spectra and in expression pattern might be another way for fish to achieve finer spatial and temporal grading of spectral sensitivity in the retina. It is of great importance to probe the functional rationale and behavioral significance of the revealed changes in expression patterns of the zebrafish M/LWS and RH2 opsin subtypes by using the power of zebrafish genetics in future studies. The results obtained in this study revealed the excellence of the zebrafish M/LWS and RH2 opsin genes for studying functional divergence of duplicated genes in a general sense and will provide the framework for subsequent studies of opsin gene regulation.
Abbreviations
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Acknowledgments |
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References |
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