New insights into the nutritional regulation of gluconeogenesis in carnivorous rainbow trout (Oncorhynchus mykiss): a gene duplication trail

Physiological Genomics - Tập 47 Số 7 - Trang 253-263 - 2015
Lucie Marandel1, Iban Seiliez1, Vincent Véron1, Sandrine Skiba‐Cassy1, Stéphane Panserat1
1Institut National de la Recherche Agronomique (INRA), Nutrition, Metabolism and Aquaculture Unit (UR1067), Saint-Pée-sur-Nivelle, France

Tóm tắt

The rainbow trout ( Oncorhynchus mykiss) is considered to be a strictly carnivorous fish species that is metabolically adapted for high catabolism of proteins and low utilization of dietary carbohydrates. This species consequently has a “glucose-intolerant” phenotype manifested by persistent hyperglycemia when fed a high-carbohydrate diet. Gluconeogenesis in adult fish is also poorly, if ever, regulated by carbohydrates, suggesting that this metabolic pathway is involved in this specific phenotype. In this study, we hypothesized that the fate of duplicated genes after the salmonid-specific 4th whole genome duplication (Ss4R) may have led to adaptive innovation and that their study might provide new elements to enhance our understanding of gluconeogenesis and poor dietary carbohydrate use in this species. Our evolutionary analysis of gluconeogenic genes revealed that pck1, pck2, fbp1a, and g6pca were retained as singletons after Ss4r, while g6pcb1, g6pcb2, and fbp1b ohnolog pairs were maintained. For all genes, duplication may have led to sub- or neofunctionalization. Expression profiles suggest that the gluconeogenesis pathway remained active in trout fed a no-carbohydrate diet. When trout were fed a high-carbohydrate diet (30%), most of the gluconeogenic genes were non- or downregulated, except for g6pbc2 ohnologs, whose RNA levels were surprisingly increased. This study demonstrates that Ss4R in trout involved adaptive innovation via gene duplication and via the outcome of the resulting ohnologs. Indeed, maintenance of ohnologous g6pcb2 pair may contribute in a significant way to the glucose-intolerant phenotype of trout and may partially explain its poor use of dietary carbohydrates.

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Tài liệu tham khảo

10.1016/0003-2697(88)90176-5

10.1016/0300-9629(79)90581-4

Bergot F, 1979, Ann Nutr Aliment, 33, 247

10.1038/ncomms4657

10.1016/0003-2697(76)90527-3

10.1038/nature13726

10.1016/j.ydbio.2006.03.018

10.2337/diabetes.49.6.969

10.1093/jn/111.2.336

10.1016/j.ygcen.2004.07.005

10.1093/nar/gkh340

10.1111/j.1432-1033.1981.tb05068.x

10.1016/j.gene.2010.10.014

10.1242/jeb.106062

10.1016/j.cbpb.2012.03.001

10.1093/jhered/esp047

Hanson RW, 1994, Adv Enzymol Relat Areas Mol Biol, 69, 203

10.1146/annurev.biochem.66.1.581

10.1079/BJN19820071

10.1093/jn/124.suppl_12.2568S

10.1016/S1095-6433(02)00267-2

10.1093/jn/133.8.2561

10.1007/s00360-007-0235-7

10.1016/j.jtbi.2005.08.033

10.1016/S0167-4781(01)00258-5

10.1534/genetics.166.2.935

10.1098/rspb.2013.2881

10.1016/j.bbagen.2012.12.013

10.1016/j.cbpc.2004.03.004

Mommsen TP, 1991, Rev Aquatic Sci, 4, 225

10.1017/S0007114508981411

10.1152/ajpregu.2000.278.5.R1164

10.1016/S0955-2863(99)00067-4

Panserat S, 2001, J Exp Biol, 204, 359, 10.1242/jeb.204.2.359

Panserat S, 2001, J Exp Biol, 204, 2351, 10.1242/jeb.204.13.2351

10.1017/S0954422414000018

10.1152/ajpregu.00120.2009

10.1002/jez.1402710603

10.1093/nar/29.9.e45

10.1016/S0014-5793(00)02020-2

10.1016/j.cbpb.2011.07.006

10.1242/jeb.050807

10.1152/ajpregu.00619.2010

10.1007/s00360-012-0658-7

10.1152/ajpregu.00369.2009

10.1534/genetics.108.090936

Rauch GJ, 2003, ZFIN

10.1159/000458816

10.1007/BF00400689

10.1186/1471-2148-9-127

Schermerhorn T, 2013, Front Endocrinol (Lausanne), 4, 188, 10.3389/fendo.2013.00188

10.1152/ajpregu.00579.2010

10.1017/S0007114512003352

10.1016/0305-0491(95)00056-E

10.1093/molbev/msr121

10.1007/s11259-005-1868-1

10.1016/S0167-4781(00)00216-5

10.1016/S0378-1119(02)00627-3

10.1016/0305-0491(95)02119-1

10.1016/j.cbpa.2013.07.013

10.1016/0305-0491(79)90015-4

10.1042/bst0110088a

10.1053/rvsc.1998.0305

10.1038/ng.3098

10.2460/javma.2002.221.1559