Type II Opsins: Evolutionary Origin by Internal Domain Duplication?

The evolutionary histories of complex traits are complicated because such traits are comprised of multiple integrated and interacting components, which may have different individual histories. Phylogenetic studies of complex trait evolution often do not take this into account, instead focusing only on the history of whole, integrated traits; for example, mapping eyes as simply present or absent through history. Using the biochemistry of animal vision as a model, we demonstrate how investigating the individual components of complex systems can aid in elucidating both the origins and diversification of such systems. Opsin-based phototransduction underlies all visual phenotypes in animals, using complex protein cascades that translate light information into changes in cyclic nucleotide gated (CNG) or canonical transient receptor potential (TRPC) ion-channel activity. Here we show that CNG ion channels play a role in cnidarian phototransduction. Transcripts of a CNG ion channel co-localize with opsin in specific cell types of the eyeless cnidarian Hydra magnipapillata. Further, the CNG inhibitor cis-diltiazem ablates a stereotypical photoresponse in the hydra. Our findings in the Cnidaria, the only non-bilaterian lineage to possess functional opsins, allow us to trace the history of CNG-based photosensitivity to the very origin of animal phototransduction. Our general analytical approach, based on explicit phylogenetic analysis of individual components, contrasts the deep evolutionary history of CNG-based phototransduction, today used in vertebrate vision, with the more recent assembly of TRPC-based systems that are common to protostome (e.g. fly and mollusc) vision.

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“…Further, type-I opsins common to bacteria and other taxa are not homologous to animal opsins (Spudich et al 2000;Larusso et al 2008).…”

Section: Discussionmentioning

confidence: 96%

The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway

2010

Self Cite

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“…Those that occur in animals are divided into seven subfamilies, all of which appear to have originated before the split between the protostomes (most invertebrates) and deuterostomes (chordates and relatives including echinoderms) (Terakita 2005;Larusso et al 2008). The extraordinary diversity of opsin molecules is likely a product of extensive gene duplication and subsequent divergence (Arendt 2003;Plachetzki and Oakley 2007;Oakley and Pankey 2008).…”

Section: Photopigments and Photoreceptorsmentioning

confidence: 98%

“…Draper (2002) has provided an abstract description that is readily applied to biological systems (including organs or biochemical pathways). In this case, a complex system with two required parts (AB) that performs a function (F) evolves through a complicated but essentially direct path involving both the addition and loss of parts:…”

Section: Scaffoldingmentioning

confidence: 99%

The Evolution of Complex Organs

Gregory

2008

Evo Edu Outreach

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The origin of complex biological structures has long been a subject of interest and debate. Two centuries ago, natural explanations for their occurrence were considered inconceivable. However, 150 years of scientific investigation have yielded a conceptual framework, abundant data, and a range of analytical tools capable of addressing this question. This article reviews the various direct and indirect evolutionary processes that contribute to the origins of complex organs. The evolution of eyes is used as a case study to illustrate these concepts, and several of the most common misconceptions about complex organ evolution are discussed.

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“…Sequence analysis has consistently failed to detect significant similarities between these rhodopsin families. Furthermore, type I rhodopsins purportedly contain a weak internal sequence repeat between helices A–C and E–G, suggestive of an ancient gene duplication event; type II rhodopsins apparently lack such an internal repeat (Taylor and Agarwal 1993; Larusso et al 2008). The two families are also taxonomically distinct.…”

Section: Introductionmentioning

confidence: 99%

An Empirical Test of Convergent Evolution in Rhodopsins

Mackin

Roy

Theobald

2013

Molecular Biology and Evolution

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Rhodopsins are photochemically reactive membrane proteins that covalently bind retinal chromophores. Type I rhodopsins are found in both prokaryotes and eukaryotic microbes, whereas type II rhodopsins function as photoactivated G-protein coupled receptors (GPCRs) in animal vision. Both rhodopsin families share the seven transmembrane α-helix GPCR fold and a Schiff base linkage from a conserved lysine to retinal in helix G. Nevertheless, rhodopsins are widely cited as a striking example of evolutionary convergence, largely because the two families lack detectable sequence similarity and differ in many structural and mechanistic details. Convergence entails that the shared rhodopsin fold is so especially suited to photosensitive function that proteins from separate origins were selected for this architecture twice. Here we show, however, that the rhodopsin fold is not required for photosensitive activity. We engineered functional bacteriorhodopsin variants with novel folds, including radical noncircular permutations of the α-helices, circular permutations of an eight-helix construct, and retinal linkages relocated to other helices. These results contradict a key prediction of convergence and thereby provide an experimental attack on one of the most intractable problems in molecular evolution: how to establish structural homology for proteins devoid of discernible sequence similarity.

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Type II Opsins: Evolutionary Origin by Internal Domain Duplication?

Cited by 34 publications

References 24 publications

The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway

The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway

The Evolution of Complex Organs

An Empirical Test of Convergent Evolution in Rhodopsins

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