Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision

Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We inv...

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Bibliographic Details
Published ineLife Vol. 7
Main Authors Castiglione, Gianni M, Chang, Belinda Sw
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 26.10.2018
eLife Sciences Publications, Ltd
Subjects
Adaptation, Biological
Animals
Binding sites
Biochemistry and Chemical Biology
Biological Evolution
Biology
Epistasis
Epistasis, Genetic
Evolution
Evolutionary Biology
Fiber optics
intramolecular epistasis
Light
Photopigments
Photosensitivity
Pigments
protein evolution
Proteins
Rhodopsin
Rhodopsin - genetics
Selection, Genetic
Vertebrates
Vision
Vision, Ocular - physiology
Canada
rhodopsin
evolutionary biology
chemical biology
protein evolution
biochemistry
none
intramolecular epistasis
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Abstract Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved E122, but instead, selection appears to have entrenched E122 in tetrapods epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed-not even for improvements to rod photosensitivity.
AbstractList Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed-not even for improvements to rod photosensitivity.
Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved E122, but instead, selection appears to have entrenched E122 in tetrapods epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed-not even for improvements to rod photosensitivity.
Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed—not even for improvements to rod photosensitivity. People can see in dim light because of cells at the back of the eye known as rods. These cells contain two key components: molecules called retinal, which are bound to proteins called rhodopsin. When light hits a rod cell, it kicks off a cascade of reactions beginning with the retinal molecule changing into an activated shape and ending with a nerve impulse travelling to the brain. The activated form of retinal is toxic, and as long as it remains bound to the rhodopsin protein it will not damage the rod or surrounding cells. The toxic retinal also cannot respond to light. It must be released from the protein and converted back to its original shape to restore dim light vision. As with all proteins, rhodopsin’s structure comprises a chain of building blocks called amino acids. Every land animal with a backbone has the same amino acid at position 122 in its rhodopsin. This amino acid, named E122, helps to stabilize the activated rhodopsin, slowing the release of the toxic retinal. Yet E122 also makes the rod cells less sensitive, resulting in poorer vision in dim light. In contrast, some fish do not have E122 but rather one of several different amino acids takes its place. What remains unclear is why all land animals have stuck with E122, and whether there were other options that evolution could have explored to overcome the trade-off between sensitivity and stability. By looking at the make-up of rhodopsins from many animals, Castiglione and Chang found other sites in the protein where the amino acid changed whenever position 122 changed. The amino acids at these so-called “coevolving sites” were then swapped into the version of rhodopsin that is found in cows, which had also been engineered to lack E122. These changes fully compensated for the destabilizing loss of E122 on activated rhodopsin but without sacrificing its sensitivity to light. Further experiments then confirmed that unless all amino acids were substituted at once, the activated rhodopsin was very unstable. Indeed, it was almost as unstable as mutated rhodopsins found in some human diseases. These findings suggest that, while there was in principle another solution available to land animals, the routes to it were closed off because they all came with an increased risk of eye disease. These findings highlight that rhodopsin likely plays a more important role in protecting humans and many other land animals against eye disease than previously assumed. More knowledge about this protective role may lead to new therapies for these conditions. Also, investigating similar evolutionary trade-offs could help to explain how and why different proteins work the way that they do today.
Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to adaptation. This may be enhanced by natural environmental variation, but in multicellular organisms this process is poorly understood. We investigated a paradoxical trajectory taken during the evolution of tetrapod dim-light vision, where in the rod visual pigment rhodopsin, E122 was fixed 350 million years ago, a residue associated with increased active-state (MII) stability but greatly diminished rod photosensitivity. Here, we demonstrate that high MII stability could have likely evolved without E122, but instead, selection appears to have entrenched E122 in tetrapods via epistatic interactions with nearby coevolving sites. In fishes by contrast, selection may have exploited these epistatic effects to explore alternative trajectories, but via indirect routes with low MII stability. Our results suggest that within tetrapods, E122 and high MII stability cannot be sacrificed—not even for improvements to rod photosensitivity. People can see in dim light because of cells at the back of the eye known as rods. These cells contain two key components: molecules called retinal, which are bound to proteins called rhodopsin. When light hits a rod cell, it kicks off a cascade of reactions beginning with the retinal molecule changing into an activated shape and ending with a nerve impulse travelling to the brain. The activated form of retinal is toxic, and as long as it remains bound to the rhodopsin protein it will not damage the rod or surrounding cells. The toxic retinal also cannot respond to light. It must be released from the protein and converted back to its original shape to restore dim light vision. As with all proteins, rhodopsin’s structure comprises a chain of building blocks called amino acids. Every land animal with a backbone has the same amino acid at position 122 in its rhodopsin. This amino acid, named E122, helps to stabilize the activated rhodopsin, slowing the release of the toxic retinal. Yet E122 also makes the rod cells less sensitive, resulting in poorer vision in dim light. In contrast, some fish do not have E122 but rather one of several different amino acids takes its place. What remains unclear is why all land animals have stuck with E122, and whether there were other options that evolution could have explored to overcome the trade-off between sensitivity and stability. By looking at the make-up of rhodopsins from many animals, Castiglione and Chang found other sites in the protein where the amino acid changed whenever position 122 changed. The amino acids at these so-called “coevolving sites” were then swapped into the version of rhodopsin that is found in cows, which had also been engineered to lack E122. These changes fully compensated for the destabilizing loss of E122 on activated rhodopsin but without sacrificing its sensitivity to light. Further experiments then confirmed that unless all amino acids were substituted at once, the activated rhodopsin was very unstable. Indeed, it was almost as unstable as mutated rhodopsins found in some human diseases. These findings suggest that, while there was in principle another solution available to land animals, the routes to it were closed off because they all came with an increased risk of eye disease. These findings highlight that rhodopsin likely plays a more important role in protecting humans and many other land animals against eye disease than previously assumed. More knowledge about this protective role may lead to new therapies for these conditions. Also, investigating similar evolutionary trade-offs could help to explain how and why different proteins work the way that they do today.
Author Castiglione, Gianni M
Chang, Belinda Sw
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  surname: Chang
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  organization: Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Canada
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30362942$$D View this record in MEDLINE/PubMed
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Keywords rhodopsin
evolutionary biology
chemical biology
protein evolution
biochemistry
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intramolecular epistasis
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License 2018, Castiglione et al.
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Department of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, United States.
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SSID ssj0000748819
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Snippet Trade-offs between protein stability and activity can restrict access to evolutionary trajectories, but widespread epistasis may facilitate indirect routes to...
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pubmedcentral
proquest
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
SubjectTerms Adaptation, Biological
Animals
Binding sites
Biochemistry and Chemical Biology
Biological Evolution
Biology
Epistasis
Epistasis, Genetic
Evolution
Evolutionary Biology
Fiber optics
intramolecular epistasis
Light
Photopigments
Photosensitivity
Pigments
protein evolution
Proteins
Rhodopsin
Rhodopsin - genetics
Selection, Genetic
Vertebrates
Vision
Vision, Ocular - physiology
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Title Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision
URI https://www.ncbi.nlm.nih.gov/pubmed/30362942
https://www.proquest.com/docview/2140014636
https://search.proquest.com/docview/2126915131
https://pubmed.ncbi.nlm.nih.gov/PMC6203435
https://doaj.org/article/2139e218d8f54a10b6eac83984b906b3
Volume 7
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