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Diversity and evolution of coral fluorescent proteins.

Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miller DJ, Wiedenmann J, Salih A, Matz MV - PLoS ONE (2008)

Bottom Line: Both proteins were green such as found elsewhere outside class Anthozoa.Interestingly, a substantial fraction of the all-coral ancestral protein had a chromohore apparently locked in a non-fluorescent neutral state, which may reflect the transitional stage that enabled rapid color diversification early in the history of coral FPs.Our results highlight the extent of convergent or parallel evolution of the color diversity in corals, provide the foundation for experimental studies of evolutionary processes that led to color diversification, and enable a comparative analysis of structural determinants of different colors.

View Article: PubMed Central - PubMed

Affiliation: Section of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America.

ABSTRACT
GFP-like fluorescent proteins (FPs) are the key color determinants in reef-building corals (class Anthozoa, order Scleractinia) and are of considerable interest as potential genetically encoded fluorescent labels. Here we report 40 additional members of the GFP family from corals. There are three major paralogous lineages of coral FPs. One of them is retained in all sampled coral families and is responsible for the non-fluorescent purple-blue color, while each of the other two evolved a full complement of typical coral fluorescent colors (cyan, green, and red) and underwent sorting between coral groups. Among the newly cloned proteins are a "chromo-red" color type from Echinopora forskaliana (family Faviidae) and pink chromoprotein from Stylophora pistillata (Pocilloporidae), both evolving independently from the rest of coral chromoproteins. There are several cyan FPs that possess a novel kind of excitation spectrum indicating a neutral chromophore ground state, for which the residue E167 is responsible (numeration according to GFP from A. victoria). The chromoprotein from Acropora millepora is an unusual blue instead of purple, which is due to two mutations: S64C and S183T. We applied a novel probabilistic sampling approach to recreate the common ancestor of all coral FPs as well as the more derived common ancestor of three main fluorescent colors of the Faviina suborder. Both proteins were green such as found elsewhere outside class Anthozoa. Interestingly, a substantial fraction of the all-coral ancestral protein had a chromohore apparently locked in a non-fluorescent neutral state, which may reflect the transitional stage that enabled rapid color diversification early in the history of coral FPs. Our results highlight the extent of convergent or parallel evolution of the color diversity in corals, provide the foundation for experimental studies of evolutionary processes that led to color diversification, and enable a comparative analysis of structural determinants of different colors.

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Analysis of ancestral proteins.A: alignment of the amino acid sequences of the reconstructed ancestral variants, five corresponding to All-coral ancestor (all-cor, 0 to 4) and five corresponding to All-Faviina ancestor (all-fav, 0 to 4). B: Unrooted neighbor-joining tree illustrating the degree of divergence between the synthesized ancestral sequences. C–E: absorbance, excitation, and emission spectra of a representative all-coral ancestor (black curves) and all-Faviina ancestor (red curves).
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pone-0002680-g003: Analysis of ancestral proteins.A: alignment of the amino acid sequences of the reconstructed ancestral variants, five corresponding to All-coral ancestor (all-cor, 0 to 4) and five corresponding to All-Faviina ancestor (all-fav, 0 to 4). B: Unrooted neighbor-joining tree illustrating the degree of divergence between the synthesized ancestral sequences. C–E: absorbance, excitation, and emission spectra of a representative all-coral ancestor (black curves) and all-Faviina ancestor (red curves).

Mentions: The sampled ancestral sequences corresponding to the all-coral ancestor differed between each other by 8–12%, all-Faviina sequences by 6–9% (Fig. 3 A, B). Despite these sequence differences, all the reconstructed variants exhibited practically identical fluorescence and absorbance phenotypes per ancestral node, with positions of the major peaks matching within 2 nm. This result indicates that the uncertainties of the ancestral sequence prediction did not affect the reconstructed ancestral phenotypes.


Diversity and evolution of coral fluorescent proteins.

Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miller DJ, Wiedenmann J, Salih A, Matz MV - PLoS ONE (2008)

Analysis of ancestral proteins.A: alignment of the amino acid sequences of the reconstructed ancestral variants, five corresponding to All-coral ancestor (all-cor, 0 to 4) and five corresponding to All-Faviina ancestor (all-fav, 0 to 4). B: Unrooted neighbor-joining tree illustrating the degree of divergence between the synthesized ancestral sequences. C–E: absorbance, excitation, and emission spectra of a representative all-coral ancestor (black curves) and all-Faviina ancestor (red curves).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2481297&req=5

pone-0002680-g003: Analysis of ancestral proteins.A: alignment of the amino acid sequences of the reconstructed ancestral variants, five corresponding to All-coral ancestor (all-cor, 0 to 4) and five corresponding to All-Faviina ancestor (all-fav, 0 to 4). B: Unrooted neighbor-joining tree illustrating the degree of divergence between the synthesized ancestral sequences. C–E: absorbance, excitation, and emission spectra of a representative all-coral ancestor (black curves) and all-Faviina ancestor (red curves).
Mentions: The sampled ancestral sequences corresponding to the all-coral ancestor differed between each other by 8–12%, all-Faviina sequences by 6–9% (Fig. 3 A, B). Despite these sequence differences, all the reconstructed variants exhibited practically identical fluorescence and absorbance phenotypes per ancestral node, with positions of the major peaks matching within 2 nm. This result indicates that the uncertainties of the ancestral sequence prediction did not affect the reconstructed ancestral phenotypes.

Bottom Line: Both proteins were green such as found elsewhere outside class Anthozoa.Interestingly, a substantial fraction of the all-coral ancestral protein had a chromohore apparently locked in a non-fluorescent neutral state, which may reflect the transitional stage that enabled rapid color diversification early in the history of coral FPs.Our results highlight the extent of convergent or parallel evolution of the color diversity in corals, provide the foundation for experimental studies of evolutionary processes that led to color diversification, and enable a comparative analysis of structural determinants of different colors.

View Article: PubMed Central - PubMed

Affiliation: Section of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America.

ABSTRACT
GFP-like fluorescent proteins (FPs) are the key color determinants in reef-building corals (class Anthozoa, order Scleractinia) and are of considerable interest as potential genetically encoded fluorescent labels. Here we report 40 additional members of the GFP family from corals. There are three major paralogous lineages of coral FPs. One of them is retained in all sampled coral families and is responsible for the non-fluorescent purple-blue color, while each of the other two evolved a full complement of typical coral fluorescent colors (cyan, green, and red) and underwent sorting between coral groups. Among the newly cloned proteins are a "chromo-red" color type from Echinopora forskaliana (family Faviidae) and pink chromoprotein from Stylophora pistillata (Pocilloporidae), both evolving independently from the rest of coral chromoproteins. There are several cyan FPs that possess a novel kind of excitation spectrum indicating a neutral chromophore ground state, for which the residue E167 is responsible (numeration according to GFP from A. victoria). The chromoprotein from Acropora millepora is an unusual blue instead of purple, which is due to two mutations: S64C and S183T. We applied a novel probabilistic sampling approach to recreate the common ancestor of all coral FPs as well as the more derived common ancestor of three main fluorescent colors of the Faviina suborder. Both proteins were green such as found elsewhere outside class Anthozoa. Interestingly, a substantial fraction of the all-coral ancestral protein had a chromohore apparently locked in a non-fluorescent neutral state, which may reflect the transitional stage that enabled rapid color diversification early in the history of coral FPs. Our results highlight the extent of convergent or parallel evolution of the color diversity in corals, provide the foundation for experimental studies of evolutionary processes that led to color diversification, and enable a comparative analysis of structural determinants of different colors.

Show MeSH
Related in: MedlinePlus