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Diversity and evolution of coral fluorescent proteins

Diversity and evolution of coral fluorescent proteins
Diversity and evolution of coral fluorescent proteins
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.

Green fluorescent protein, RFP, Red fluorescent protein, Light sensing, Coral health
1932-6203
e2680
Alieva, N.O.
dfa0004f-8a5f-47dc-b936-9d19e8fd2e3a
Konzen, K.A.
ee0571bc-6930-48cf-9752-960ed1b56a5e
Field, S.F.
65417123-b278-49df-aeb0-b83c94398b97
Meleshkevitch, E.A.
713d69d0-e952-4646-bb3a-8c90d3a953c4
Hunt, M.
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Beltran-Ramirez, V.
4e209e66-8745-4864-85e3-32c8e6088d15
Nienhaus, G-U.
4d9a271a-da1b-43dc-af34-d2675e6b1090
Miller, D.J.
a230d4ba-cdd8-4e3b-8d96-3bc31863b7a8
Wiedenmann, J.
ad445af2-680f-4927-90b3-589ac9d538f7
Salih, A.
20176292-4829-4e28-bac4-b0e7e22ba64a
Matz, M.V.
c8e03eb9-ac39-455d-98ce-1f57f00c5596
Alieva, N.O.
dfa0004f-8a5f-47dc-b936-9d19e8fd2e3a
Konzen, K.A.
ee0571bc-6930-48cf-9752-960ed1b56a5e
Field, S.F.
65417123-b278-49df-aeb0-b83c94398b97
Meleshkevitch, E.A.
713d69d0-e952-4646-bb3a-8c90d3a953c4
Hunt, M.
1b751b4a-3491-4dec-8d45-a27269566d3a
Beltran-Ramirez, V.
4e209e66-8745-4864-85e3-32c8e6088d15
Nienhaus, G-U.
4d9a271a-da1b-43dc-af34-d2675e6b1090
Miller, D.J.
a230d4ba-cdd8-4e3b-8d96-3bc31863b7a8
Wiedenmann, J.
ad445af2-680f-4927-90b3-589ac9d538f7
Salih, A.
20176292-4829-4e28-bac4-b0e7e22ba64a
Matz, M.V.
c8e03eb9-ac39-455d-98ce-1f57f00c5596

Alieva, N.O., Konzen, K.A., Field, S.F., Meleshkevitch, E.A., Hunt, M., Beltran-Ramirez, V., Nienhaus, G-U., Miller, D.J., Wiedenmann, J., Salih, A. and Matz, M.V. (2008) Diversity and evolution of coral fluorescent proteins. PLoS ONE, 3 (7), e2680. (doi:10.1371/journal.pone.0002680).

Record type: Article

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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Published date: 2008
Keywords: Green fluorescent protein, RFP, Red fluorescent protein, Light sensing, Coral health
Organisations: Ocean and Earth Science

Identifiers

Local EPrints ID: 58247
URI: https://eprints.soton.ac.uk/id/eprint/58247
ISSN: 1932-6203
PURE UUID: ccd684ba-8a4c-4893-a4a7-a17ad21ebd87
ORCID for J. Wiedenmann: ORCID iD orcid.org/0000-0003-2128-2943

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Date deposited: 12 Aug 2008
Last modified: 12 Nov 2019 01:45

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Contributors

Author: N.O. Alieva
Author: K.A. Konzen
Author: S.F. Field
Author: E.A. Meleshkevitch
Author: M. Hunt
Author: V. Beltran-Ramirez
Author: G-U. Nienhaus
Author: D.J. Miller
Author: J. Wiedenmann ORCID iD
Author: A. Salih
Author: M.V. Matz

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