Advertisement

Visual cells and visual pigments of the river lamprey revisited

Abstract

Retinas of the river lamprey Lampetra fluviatilis were studied by microspectrophotometry, electroretinography and single-photoreceptor electrophysiology to reconcile the apparently contradictory conclusions on the nature of lamprey photoreceptor cells drawn in the early work by Govardovskii and Lychakov (J Comp Physiology A 154:279–286, 1984) and in recent studies. In agreement with recent works, we confirmed former identification of short photoreceptors as rods and of long photoreceptors as cones. In line with the results of 1984, we show that within a certain range of light intensities the lamprey retina exhibits “color discrimination”. We found that the overlap of working intensity ranges of rods and cones is not a unique feature of lamprey short receptors, and suggest that rod-cone (possibly color) vision may be common among vertebrates. We show that the decay of meta-intermediates in lamprey cones occurs almost 100 times faster than in typical rod metarhodopsins. Rate of decay of metarhodopsins of lamprey rods take an intermediate position between typical rods and cones. This makes lamprey rhodopsin similar to transmuted cone visual pigment in “rods” of nocturnal geckos. We argue that defining various types of photoreceptors as simply “rods” and “cones” may be functionally correct, but neglects their genetic, biochemical and morphological features and evolutionary history.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Abbreviations

RvI :

Response vs. Intensity curve

References

  1. Astakhova LA, Firsov ML, Govardovskii VI (2008) Kinetics of turnoffs of frog rod phototransduction cascade. J Gen Physiol 132(5):587–604 (PMID: 18955597)

  2. Astakhova LA, Firsov ML, Govardovskii VI (2015) Activation and quenching of the phototransduction cascade in retinal cones as inferred from electrophysiology and mathematical modeling. Mol Vis 21:244–263 (PMID: 25866462)

  3. Asteriti S, Grillner S, Cangiano L (2015) A Cambrian origin for vertebrate rods. Elife 4:e07166 (PMID: 26095697)

  4. Baylor DA, Lamb TD, Yau KW (1979) Responses of retinal rods to single photons. J Physiol 288:613–634 (PMID: 112243)

  5. Bowmaker JK, Govardovskii VI, Shukolyukov SA, Zueva LV, Hunt DM, Sideleva VG, Smirnova OG (1994) Visual pigments and the photic environment: the cottoid fish of Lake Baikal. Vision Res 34(5):591–605 (PMID: 8160379)

  6. Bridges CDB (1972) The rhodopsin–porphyropsin visual system. In: Dartnall HJA (ed) Handbook of sensory physiology VII. Springer, Berlin, pp 417–480. https://doi.org/10.1007/978-3-642-65066-6_11

  7. Collin SP, Hart NS, Shand J, Potter IC (2003a) Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis). Vis Neurosci 20(2):119–130 (PMID: 12916734)

  8. Collin SP, Knight MA, Davies WL, Potter IC, Hunt DM, Trezise AE (2003b) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13(22):R864–R865 (PMID: 14614838)

  9. Collin SP, Trezise AEO (2006) Response to Pisani. Curr Biology 16(9):R320

  10. Crescitelli F (1977) The visual pigments of geckos and other vertebrates: an essay in comparative biology. In: Crescitelli F (ed) Handbook of sensory physiology, vol 7/5. Springer, Berlin, pp 391–450. https://doi.org/10.1007/978-3-642-66468-7_7

  11. Davies WL, Cowing JA, Carvalho LS, Potter IC, Trezise AE, Hunt DM, Collin SP (2007) Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J 21:2713–2724. https://doi.org/10.1096/fj.06-8057com

  12. Davies WL, Collin SP, Hunt DM (2009) Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol Biol Evol 26(8):1803–1809. https://doi.org/10.1093/molbev/msp089

  13. Dickson DH, Graves DA (1979) Fine structure of the lamprey photoreceptors and retinal pigment epithelium (Petromyzon marinus L). Exp Eye Res 29(1):45–60 (PMID: 228957)

  14. Enright JM, Toomey MB, Sato SY, Temple SE, Allen JR, Fujiwara R, Kramlinger VM, Nagy LD, Johnson KM, Xiao Y, How MJ, Johnson SL, Roberts NW, Kefalov VJ, Guengerich FP, Corbo JC (2015) Cyp27c1 red-shifts the spectral sensitivity of photoreceptors by converting vitamin A1 into A2. Curr Biol 25(23):3048–3057 (PMID: 26549260)

  15. Estevez ME, Kolesnikov AV, Ala-Laurila P, Crouch RK, Govardovskii VI, Cornwall MC (2009) The 9-methyl group of retinal is essential for rapid Meta II decay and phototransduction quenching in red cones. J Gen Physiol 134(2):137–150 (PMID: 19635855)

  16. Fain GL (2019) Lamprey vision: photoreceptors and organization of the retina. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2019.10.008

  17. Golobokova EYu, Govardovskii VI (2006) Late stages of visual pigment photolysis in situ: cones vs. rods. Vision Res 46(14):2287–2297 (PMID: 16473387)

  18. Govardovskii VI (1975) On the sites of generation of the early and late receptor potentials in rods. Vision Res 15:971–986 (PMID: 1172644)

  19. Govardovskii VI, Lychakov DV (1984) Visual cells and visual pigments of the lamprey, Lampetra fluviatilis. J Comp Physiology A 154:279–286. https://doi.org/10.1007/BF00604994

  20. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17(4):509–528 (PMID: 11016572)

  21. Hárosi FI, Kleinschmidt J (1993) Visual pigments in the sea lamprey, Petromyzon marinus. Vis Neurosci 10(4):711–715 (PMID: 8338808)

  22. Hofmann KP (2000) Late photoproducts and signaling states of bovine rhodopsin. In: Stavenga DG, DeGrip WJ, Pugh EN Jr (eds) Handbook of biological physics, vol 3, chapter 3. Elsevier Science B.V., North Holland, pp 91–142

  23. Imai H, Kuwayama S, Onishi A, Morizumi T, Chisaka O, Shichida Y (2005) Molecular properties of rod and cone visual pigments from purified chicken cone pigments to mouse rhodopsin in situ. Photochem Photobiol Sci 4:667–674 (PMID: 16121275)

  24. Knowles A, Dartnall HJA (1977) The photobiology of vision. In: Davson H (ed) The eye, vol 2B. Academic Press, London-New York, pp 53–101. (ISBN 0122067622,9780122067624)

  25. Kolesnikov AV, Golobokova EYu, Govardovskii VI (2003) The identity of metarhodopsin III. Visual Neurosci 20(3):249–265 [PMID: 14570247]

  26. Kolesnikov AV, Ala-Laurila P, Shukolyukov SA, Crouch RK, Wiggert B, Estevez ME, Govardovskii VI, Cornwall MC (2007) Visual cycle and its metabolic support in gecko photoreceptors. Vision Res 47(3):363–374 (PMID: 17049961)

  27. Korenyak DA, Govardovskii VI (2012) Temperature dependence of slow stages of rhodopsin photolysis in intact rods of frog and rat retina. Sensory Systems 26(2):141–149. In Russian. [UDC: 612.843.116.1; ISSN: 0235-0092]

  28. Lamb TD (2013) Evolution of phototransduction, vertebrate photoreceptors and retina. Prog Retin Eye Res 36:52–119 [PMID: 23792002]

  29. Laties AM, Bok D, Liebman P (1976) Procion yellow: a marker dye for outer segment disc patency and for rod renewal. Exp Eye Res 23(2):139–148 [PMID: 61886]

  30. Loew ER, Govardovskii VI, Rōhlich P, Szel A (1996) Microspectrophotometric and immunocytochemical identification of ultraviolet photoreceptors in geckos. Visual Neurosci 13(2):247–256 [PMID: 8737275]

  31. Lychakov DV (1976) Light- and electronmicroscopic study of photoreceptors of the lamprey, Lampetra fluviatilis. J Evol Biochem Physiol 12:358–361. (In Russian)

  32. Lythgoe JN (1979) The ecology of vision. Clarendon Press, Oxford. (ISBN 0198545290)

  33. Morshedian A, Fain GL (2015) Single-photon sensitivity of lamprey rods with cone-like outer segments. Curr Biol 25(4):484–487 (PMID: 25660538)

  34. Morshedian A, Fain GL (2017) Light adaptation and the evolution of vertebrate photoreceptors. J Physiol 595(14):4947–4960 (PMID: 28488783)

  35. Morshedian A, Toomey MB, Pollock GE, Frederiksen R, Enright JM, McCormick SD, Cornwall MC, Fain GL, Corbo JC (2017) Cambrian origin of the CYP27C1-mediated vitamin A1-to-A2 switch, a key mechanism of vertebrate sensory plasticity. R Soc Open Sci 4(7):70362 (PMID: 28791166)

  36. Muradov H, Kerov V, Boyd KK, Artemyev NO (2008) Unique transducins expressed in long and short photoreceptors of lamprey Petromyzon marinus. Vision Res 48(21):2302–2308 (PMID: 18687354)

  37. Öhman P (1971) The photoreceptor outer segments of the river lamprey (Lampreta fluviatilis). An electron- fluorescence- and light microscopic study. Acta Zool 52:287–297. https://doi.org/10.1111/j.1463-6395.1971.tb00564.x

  38. Öhman P (1976) Fine structure of photoreceptors and associated neurons in the retina of Lampetra fluviatilis (Cyclostomi). Vision Res 16(6):659–662 (PMID: 960589)

  39. Pinto BJ, Nielsen SV, Gamble T (2019) Transcriptomic data support a nocturnal bottleneck in the ancestor of gecko lizards. Mol Phylogenet Evolution 141:106639 [PMID: 31586687]

  40. Pisani D, Mohun SM, Harris SR, MacInerney JO, Wilkinson M (2006) Molecular evidence for dim-light vision in the last common ancestor of the vertebrates. Curr Biology 16(9):R318–R319 (PMID: 16682336)

  41. Sakurai K (2017) Physiological characteristics of photoreceptors in the lamprey, Lethenteron japonicum. Zoolog Sci 34(4):326–330 (PMID: 28770673)

  42. Schott RK, Bhattacharyya N, Chang BSW (2019) Evolutionary signatures of photoreceptor transmutation in geckos reveal potential adaptation and convergence with snakes. Evolution 73(9):1958–1971 [PMID: 31339168]

  43. Tretjakoff DK (1916) Sense organs of the river lamprey. Transactions of Novoross Univ, Phys Mat Fac 8, Odessa

  44. Wald G (1957) The metamorphosis of visual systems in the sea lamprey. J Gen Physiol 40(6):901–914 [PMID: 13439167]

  45. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Press, Bloomfield Hills, pp 1–818. https://doi.org/10.1002/ar.1090880409

  46. Yanagawa M, Kojima K, Yamashita T, Imamoto Y, Matsuyama T, Nakanishi K, Yamano Y, Wada A, Sako Y, Shichida Y (2015) Origin of the low thermal isomerization rate of rhodopsin chromophore. Sci Rep 5:11081 (PMID: 26061742)

  47. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog in Retin Eye Res 19(4):385–419 [PMID: 10785616]

  48. Yokoyama S, Blow NS (2001) Molecular evolution of the cone visual pigments in the pure rod-retina of the nocturnal gecko. Gekko gecko. Gene 276(12):117–125 [PMID: 11591478]

  49. Young RW (1969) A difference between rods and cones in the renewal of outer segment protein. Invest Ophthalmol 8(2):222–231 (PMID: 5777484)

  50. Zhang X, Wensel TG, Yuan C (2006) Tokay gecko photoreceptors achieve rod-like physiology with cone-like proteins. Photochem Photobiol 82(6):1452–1460 (PMID: 16553462)

Download references

Acknowledgements

The work was supported by the Russian Government program No 075-00776-19-02. Authors are thankful to Prof. K.K. Donner for help with English text. All experimental animals were treated in accordance with the European Communities Council Directive (24th November 1986; 86/609/EEC) and the protocol was approved by the local Institutional Animal Care and Use Committee.

Author information

Correspondence to Victor Govardovskii.

Ethics declarations

Conflict of interest

Authors declare no conflict of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Govardovskii, V., Rotov, A., Astakhova, L. et al. Visual cells and visual pigments of the river lamprey revisited. J Comp Physiol A (2020). https://doi.org/10.1007/s00359-019-01395-5

Download citation

Keywords

  • Lamprey
  • Rods
  • Cones
  • Electrophysiology
  • Visual pigments