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Loss of genes implicated in gastric function during platypus evolution

Gonzalo R Ordoñez1, LaDeana W Hillier2, Wesley C Warren2, Frank Grützner3, Carlos López-Otín1 and Xose S Puente1*

Author Affiliations

1 Departamento de Bioquímica y Biología Molecular, Facultad de Medicina, Instituto Universitario de Oncología, Universidad de Oviedo, C/Fernando Bongera s/n, 33006 Oviedo, Spain

2 Genome Sequencing Center, Washington University School of Medicine, Campus Box 8501, 4444 Forest Park Avenue, St. Louis, Missouri 63108, USA

3 Discipline of Genetics, School of Molecular & Biomedical Science, The University of Adelaide, 5005 South Australia, Adelaide, Australia

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Genome Biology 2008, 9:R81  doi:10.1186/gb-2008-9-5-r81

Published: 15 May 2008

Abstract

Background

The duck-billed platypus (Ornithorhynchus anatinus) belongs to the mammalian subclass Prototheria, which diverged from the Theria line early in mammalian evolution. The platypus genome sequence provides a unique opportunity to illuminate some aspects of the biology and evolution of these animals.

Results

We show that several genes implicated in food digestion in the stomach have been deleted or inactivated in platypus. Comparison with other vertebrate genomes revealed that the main genes implicated in the formation and activity of gastric juice have been lost in platypus. These include the aspartyl proteases pepsinogen A and pepsinogens B/C, the hydrochloric acid secretion stimulatory hormone gastrin, and the α subunit of the gastric H+/K+-ATPase. Other genes implicated in gastric functions, such as the β subunit of the H+/K+-ATPase and the aspartyl protease cathepsin E, have been inactivated because of the acquisition of loss-of-function mutations. All of these genes are highly conserved in vertebrates, reflecting a unique pattern of evolution in the platypus genome not previously seen in other mammalian genomes.

Conclusion

The observed loss of genes involved in gastric functions might be responsible for the anatomical and physiological differences in gastrointestinal tract between monotremes and other vertebrates, including small size, lack of glands, and high pH of the monotreme stomach. This study contributes to a better understanding of the mechanisms that underlie the evolution of the platypus genome, might extend the less-is-more evolutionary model to monotremes, and provides novel insights into the importance of gene loss events during mammalian evolution.