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Open Access Highly Accessed Research article

Expression profiling of rainbow trout testis development identifies evolutionary conserved genes involved in spermatogenesis

Antoine D Rolland1, Jean-Jacques Lareyre1, Anne-Sophie Goupil1, Jérôme Montfort1, Marie-Jo Ricordel1, Diane Esquerré234, Karine Hugot234, Rémi Houlgatte5, Fréderic Chalmel6 and Florence Le Gac1*

Author Affiliations

1 INRA, UR1037, IFR-140, Ouest Genopole, Rennes, 35042, France

2 INRA, UMR 1313 de Génétique Animale et Biologie Intégrative, Domaine de Vilvert, 78350 Jouy-en-Josas, France

3 CEA, DSV, iRCM, SREIT, Laboratoire de Génétique Animale et Biologie Intégrative, 78350 Jouy-en-Josas, France

4 AgroParisTech, UMR de Génétique Animale et Biologie Intégrative, 78350 Jouy-en-Josas, France

5 Inserm, U915, Université de Nantes, Faculté de Médecine, Nantes, 44035, France

6 Inserm, U625, GERHM, Université de Rennes1, IFR-140, Ouest Genopole, Rennes, 35042, France

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BMC Genomics 2009, 10:546  doi:10.1186/1471-2164-10-546

Published: 20 November 2009

Abstract

Background

Spermatogenesis is a late developmental process that involves a coordinated expression program in germ cells and a permanent communication between the testicular somatic cells and the germ-line. Current knowledge regarding molecular factors driving male germ cell proliferation and differentiation in vertebrates is still limited and mainly based on existing data from rodents and human. Fish with a marked reproductive cycle and a germ cell development in synchronous cysts have proven to be choice models to study precise stages of the spermatogenetic development and the germ cell-somatic cell communication network. In this study we used 9K cDNA microarrays to investigate the expression profiles underlying testis maturation during the male reproductive cycle of the trout, Oncorhynchus mykiss.

Results

Using total testis samples at various developmental stages and isolated spermatogonia, spermatocytes and spermatids, 3379 differentially expressed trout cDNAs were identified and their gene activation or repression patterns throughout the reproductive cycle were reported. We also performed a tissue-profiling analysis and highlighted many genes for which expression signals were restricted to the testes or gonads from both sexes. The search for orthologous genes in genome-sequenced fish species and the use of their mammalian orthologs allowed us to provide accurate annotations for trout cDNAs. The analysis of the GeneOntology terms therefore validated and broadened our interpretation of expression clusters by highlighting enriched functions that are consistent with known sequential events during male gametogenesis. Furthermore, we compared expression profiles of trout and mouse orthologs and identified a complement of genes for which expression during spermatogenesis was maintained throughout evolution.

Conclusion

A comprehensive study of gene expression and associated functions during testis maturation and germ cell differentiation in the rainbow trout is presented. The study identifies new pathways involved during spermatogonia self-renewal or rapid proliferation, meiosis and gamete differentiation, in fish and potentially in all vertebrates. It also provides the necessary basis to further investigate the hormonal and molecular networks that trigger puberty and annual testicular recrudescence in seasonally breeding species.