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First published online November 19, 2007
Journal of Experimental Biology 210, 4123-4135 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009217
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Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development

Christiana L. Cheng and Iñigo Novales Flamarique*

Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada, V5A 1S6


Figure 1
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  		Fig. 1. Cone mosaic formations in the light-adapted retina of adult rainbow trout. (A) Square mosaic with corner cones from the centro-dorsal retina, (B) row mosaic from the centro-temporal retina, and (C,D) square mosaic with and without corner cones from the centro-ventral and centro-nasal parts of the retina, respectively. An asterisk indicates a corner cone, a white arrowhead points to the partitioning membrane of a double cone, and `c' refers to a centre cone. (E,F) Square to row mosaics from the proximal (E) and distal (F) dorsal retina. (G,H) Square mosaics with few to no corner cones from the proximal (G) and distal (H) ventral retina. Cones are smaller and more closely packed towards the distal (peripheral) retina. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 2
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  		Fig. 2. Micrographs of sections from the smolt retina following in situ hybridization with the UV or blue riboprobes derived from coho (coUV, coBL) or rainbow trout (rtUV, rtBL). (A–D) Serial sections from the mid-ventral retina show that the UV riboprobes (coUV in A and rtUV in C) do not label any cones while the blue riboprobes (coBL in B and rtBL in D) label all single cones, regardless of position in the square mosaic. (E,F) Serial sections from the dorso-nasal periphery show multiple cells labelled by the UV riboprobes (coUV in E and rtUV in F). Black arrowheads point to unlabelled single cones, black arrows point to single cones labelled with the blue riboprobes, and white arrows point to single cones labelled with the UV riboprobes; rpe, retinal pigment epithelium. The riboprobe used in each section is specified at the bottom of each panel. Other symbols and nomenclature as in Fig. 1. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 3
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  		Fig. 3. Micrographs of sections from the adult retina following in situ hybridization with the two sets of UV and blue riboprobes. (A–D) Serial sections from the upper dorsal retina show that the UV riboprobes (coUV in A and rtUV in C) do not label any cones while the blue riboprobes (coBL in B and rtBL in D) label all single cones, regardless of position in the square mosaic. (E–H) Radial serial sections from the same area as in A–D show lack of labelling by the UV riboprobes (coUV in E and rtUV in G) and labelling of all single cones by the blue riboprobes (coBL in F and rtBL in H). Note that, in the light-adapted retina, the double cone ellipsoids (see white arrowheads pointing to the partitions) are located closer to the retinal pigment epithelium with respect to the single cones. Other symbols and nomenclature as in Fig. 2. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 4
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  		Fig. 4. Micrographs of sections from the adult retina following in situ hybridization with the UV and blue riboprobes after variable proteinase K incubation times. (A–F) Serial sections from the mid-ventro-temporal retina show that the coho UV riboprobe (coUV) does not label cones after 5 min (A,D) or 13 min (B,E) of proteinase K exposure, and this is the same result as obtained using the rainbow trout UV riboprobe (rtUV) after 13 min of proteinase K exposure (C,F). (G,H) Serial tangential (G) and radial (H) sections corresponding to those in A–F show that all single cones are labelled by the blue riboprobe (rtBL) after 10 min of proteinase K treatment. The riboprobes used and the time of proteinase K exposure (in parentheses) are shown at the bottom of each panel. Note that proteinase K exposure times used by Allison et al. (Allison et al., 2003Go) for the rainbow trout UV and blue riboprobes were 13 min and 10 min, respectively. Other symbols and nomenclature as in Fig. 2. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 5
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  		Fig. 5. Micrographs of sections from the retina of the alevin following in situ hybridization with the rainbow trout UV and blue riboprobes. (A–D) Serial sections from the dorsal retina show a full square mosaic in which all single cones are labelled by the UV riboprobe (A,C) and none are labelled with the blue riboprobe (B,D). (E–H) Serial sections from the lower ventral retina show that most single cones are labelled by the UV riboprobe (E,G) but some are also labelled with the blue riboprobe (F,H). d, double cone; other symbols and nomenclature as in Fig. 2. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 6
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  		Fig. 6. Composites of micrographs from the distal ventral retina of the alevin showing the progression of retinal development from the peripheral undifferentiated growth zone (ugz), at the top of each figure, toward the (main) central retina, at the bottom of each figure. Labelling by the UV riboprobe (rtUV, A) appears closer to the ugz than labelling by the blue riboprobe (rtBL, B). Symbols and nomenclature as in Fig. 5. Magnification bar (at the bottom right of the figure) is 25 µm.

 

Figure 7
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  		Fig. 7. Retinal maps of cone distributions in the retina of rainbow trout from the alevin to the adult (N=4 per map). (A,B) Mean cone density and percentage of single cones that express UV opsin mRNA (in brackets) in the retina of the alevin (A) and parr (B). All locations had square mosaics complete with corner cones such that d/s was ~1. The overwhelming majority of single cones in the alevin retina expressed UV opsin. Shown for the parr retina (B) are the approximate regions with cones expressing only blue opsin mRNA (blue), a combination of UV and blue opsin mRNA (mostly as corner cones expressing UV opsin mRNA and centre cones expressing blue opsin mRNA, but with some cones co-expressing the two transcripts; UV-blue), and cones expressing only UV opsin mRNA (UV). (C,D) Mean cone density and associated d/s ratio (in parentheses) in the retina of the smolt (C) and the adult (D). All single cones in the main (non-peripheral) retina expressed blue opsin mRNA. For each retina, the area within the red perimeter had high corner cone densities (d/s ratio <1.4). Cone densities are expressed in thousands per square millimetre. A larger circle indicates that the mean cone density for that location was at least 1 s.d. above the mean from all locations pooled together. A smaller circle indicates the opposite. In salmonid fishes, the embryonic fissure (ef) runs from the ventral to the central retina (approximate location of the optic nerve head), pointing toward the temporal retina. D, dorsal, N, nasal. Magnification bar is 0.11 cm in A, 0.12 cm in B, 0.33 cm in C and 0.39 cm in D.

 

Figure 8
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  		Fig. 8. Micrographs of sections from the large alevin/parr retina following double label in situ hybridization with the rainbow trout UV and blue riboprobes. (A,B). Tangential (A) and radial (B) sections from the centro-temporal retina showing single cones expressing UV opsin mRNA (red colour), blue opsin mRNA (blue colour), and both UV and blue opsin mRNAs (purple colour, green arrow). (C) Tangential section from the centro-ventral retina showing corner cones expressing UV opsin mRNA and centre cones expressing blue opsin mRNA. (D) Radial section from the nasal periphery showing single cones expressing UV or blue opsin mRNA. (E–G) Tangential (E) and radial (F) sections from the mid-dorsal retina show that all single cones express UV opsin mRNA exclusively, as do single cones from the distal dorsal retina (G). (H) Radial section from the distal temporal retina showing that the majority of cones express UV opsin mRNA, though some show early signs of co-expression (green arrow). Other symbols and nomenclature as in Fig. 5. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 9
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  		Fig. 9. Micrographs of sections from the smolt retina following in situ hybridization with the rainbow trout UV and blue riboprobes. (A,B) Serial radial sections from the distal nasal retina show that no cone is labelled with the UV riboprobe (A) and all single cones are labelled with the blue riboprobe (B). (C–E) Tangential (C) and radial (D) sections from the mid-dorsal retina show that all single cones are labelled exclusively with the blue riboprobe, as are single cones from the temporal retina (E). The sections shown in C–E were double labelled with the UV and blue riboprobes, but only the blue riboprobe showed labelling. Symbols and nomenclature as in Fig. 5. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 10
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  		Fig. 10. Micrographs of sections from smolt and adult retinas following double label in situ hybridization with the green (rtGR) and red (rtRE) riboprobes or with the UV (rtUV) and blue (rtBL) riboprobes. (A) Tangential section from the centro-temporal retina of the smolt showing that each member of a double cone expresses a mRNA encoding green opsin (blue colour) or red opsin (red colour), and that these alternate around the unit mosaic. (B) Tangential section from the centro-dorsal retina of the smolt, adjacent to the embryonic fissure, shows two faint UV riboprobe labels (though no associated cone morphology is clearly discernable) among the single cone population. (C,D) Tangential sections from the centro-dorsal (C) and centro-temporal (D) retina of adult rainbow trout showing the same labelling pattern of double cones as in the smolt retina. Symbols and nomenclature as in Fig. 5. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 11
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  		Fig. 11. Micrographs of sections from the retina of the adult following in situ hybridization with the rainbow trout UV and blue riboprobes. (A,B) Serial tangential sections from the dorsal retina show that no cone is labelled by the UV riboprobe (A) but all single cones are labelled with the blue riboprobe (B). (C–F) Tangential sections, double labelled with the UV and blue riboprobes, show exclusive labelling of all single cones by the blue riboprobe in the centro-temporal (C) and centro-ventral (D) retina, and in the temporal (E) and ventral (F) periphery. Symbols and nomenclature as in Fig. 5. Magnification bar (in A) is 25 µm and relates to all panels.

 

Figure 12
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  		Fig. 12. Absolute absorbance spectra of isolated photoreceptors in rainbow trout. (A) Single cones in the young alevin contain a visual pigment maximally sensitive to ultraviolet light (UV) while single cones in the smolt retina contain a visual pigment maximally sensitive to blue light (BL). (B) Green (G) and red (R) visual pigments present in the double cones of the smolt (one pigment per member), and rod opsin pigment (r) contained in the rods.

 

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© The Company of Biologists Ltd 2007