Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration

The evolution of teleost coloration is strongly linked with the fish-specific genome duplication (FSGD). Sepiapterin reductase (Spr) is commonly required in pteridine pigment synthesis and two paralogs are found in teleosts. However, the functions of spra and sprb in pigmentation have not been compl...

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Main Authors: X. Tian, Y.S. Shan, N.N. Peng, X. Ma, X. Shi, H. Li, X.J. Li, X.L. Meng
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Aquaculture Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352513423004398
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author X. Tian
Y.S. Shan
N.N. Peng
X. Ma
X. Shi
H. Li
X.J. Li
X.L. Meng
author_facet X. Tian
Y.S. Shan
N.N. Peng
X. Ma
X. Shi
H. Li
X.J. Li
X.L. Meng
author_sort X. Tian
collection DOAJ
description The evolution of teleost coloration is strongly linked with the fish-specific genome duplication (FSGD). Sepiapterin reductase (Spr) is commonly required in pteridine pigment synthesis and two paralogs are found in teleosts. However, the functions of spra and sprb in pigmentation have not been completely elucidated. Here we found that spra was intensively expressed in skin, fins and scales of koi carp, while sprb was ubiquitously expressed in all tissues. Then, the Spr enzyme activity inhibitor, sulfapyridine (SFD), was used to explore the phenotype and genes variation after spr inhibition. Following the administration of SFD, spra was significantly suppressed but sprb was up-regulated in skin. Additionally, the color phenotypes shifted from red to yellow due to a reduction in carotenoid concentration and the number of xanthophores/erythrophores in scales. Furthermore, the genes involved in carotenoid metabolism were influenced. However, pteridine metabolism-related genes rarely exhibited obvious changes. The results indicate that spra inhibition resulted in the dysregulation of carotenoid metabolism and pigment cells reduction, whereas sprb was likely to maintain the conserved functions in pteridine synthesis for metabolic homoeostasis. This study provided evidences for the different functions of spr paralogs in carotenoid and pteridine metabolism and for better understanding of the relationship between genome duplication and color pattern diversification.
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spelling doaj.art-047348dafbf141b4a888d9dd934425fa2024-08-21T06:30:35ZengElsevierAquaculture Reports2352-51342024-02-0134101900Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) colorationX. Tian0Y.S. Shan1N.N. Peng2X. Ma3X. Shi4H. Li5X.J. Li6X.L. Meng7College of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR ChinaCollege of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR ChinaCollege of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR ChinaCollege of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR ChinaCollege of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR ChinaHenan Academy of Fishery Sciences, Zhengzhou 450040, PR ChinaCollege of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR ChinaCollege of Fisheries, Henan Normal University, Xinxiang 453007, PR China; Engineering Technology Research Center of Henan Province for Aquatic Animal Cultivation, Henan Normal University, Xinxiang 453007, PR China; Corresponding author at: College of Fisheries, Henan Normal University, Xinxiang 453007, PR China.The evolution of teleost coloration is strongly linked with the fish-specific genome duplication (FSGD). Sepiapterin reductase (Spr) is commonly required in pteridine pigment synthesis and two paralogs are found in teleosts. However, the functions of spra and sprb in pigmentation have not been completely elucidated. Here we found that spra was intensively expressed in skin, fins and scales of koi carp, while sprb was ubiquitously expressed in all tissues. Then, the Spr enzyme activity inhibitor, sulfapyridine (SFD), was used to explore the phenotype and genes variation after spr inhibition. Following the administration of SFD, spra was significantly suppressed but sprb was up-regulated in skin. Additionally, the color phenotypes shifted from red to yellow due to a reduction in carotenoid concentration and the number of xanthophores/erythrophores in scales. Furthermore, the genes involved in carotenoid metabolism were influenced. However, pteridine metabolism-related genes rarely exhibited obvious changes. The results indicate that spra inhibition resulted in the dysregulation of carotenoid metabolism and pigment cells reduction, whereas sprb was likely to maintain the conserved functions in pteridine synthesis for metabolic homoeostasis. This study provided evidences for the different functions of spr paralogs in carotenoid and pteridine metabolism and for better understanding of the relationship between genome duplication and color pattern diversification.http://www.sciencedirect.com/science/article/pii/S2352513423004398spra/bParalogs functionCarotenoid metabolismPteridine metabolismPigmentation
spellingShingle X. Tian
Y.S. Shan
N.N. Peng
X. Ma
X. Shi
H. Li
X.J. Li
X.L. Meng
Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration
Aquaculture Reports
spra/b
Paralogs function
Carotenoid metabolism
Pteridine metabolism
Pigmentation
title Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration
title_full Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration
title_fullStr Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration
title_full_unstemmed Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration
title_short Sepiapterin reductase (Spra and Sprb) regulate carotenoid and pteridine metabolism influencing the koi carp (Cyprinus carpio L.) coloration
title_sort sepiapterin reductase spra and sprb regulate carotenoid and pteridine metabolism influencing the koi carp cyprinus carpio l coloration
topic spra/b
Paralogs function
Carotenoid metabolism
Pteridine metabolism
Pigmentation
url http://www.sciencedirect.com/science/article/pii/S2352513423004398
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