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Rethinking imprinting
Evidence of a common phenomenon in exotic pig cross
Edward R. Winstead

In the late 1980s, Dutch pig producers began mating European boars with sows from China. For the swine industry, it was a perfect match: commercial Dutch pigs have the leanness consumers want and Chinese Meishan sows produce large litters. Then, a few years ago, scientists began using the genetically diverse strains to study inheritance and gene expression. This month, Dutch researchers report that four body composition traits in pigs of mixed Dutch-Chinese descent appear to be under the influence of a phenomenon known as genomic imprinting.

"The real beauty queen among the Meishan sows," says de Koning. She had been featured in Dutch agricultural magazines.

An imprinted gene in a child or baby animal functions differently depending on which parent it is inherited from. Imprinted genes have been reported in humans, mice, and livestock animals, including pigs and sheep. (see Images of Imprinting)  Last year, researchers in Belgium and Sweden identified an imprinted chromosomal region in pigs linked to muscle mass and body fat. Assuming the region is not unique, the Dutch group systematically scanned the genomes of their pig population for signs of imprinting.

The scans revealed five regions in the pig genome that significantly affect body composition, four of which are imprinted. "We found very strong effects of imprinting for body composition traits," says Dirk-Jan de Koning, of the Institute of Animal Sciences at Wageningen University in The Netherlands. The traits, such as back-fat thickness and muscle depth, are thought to involve many genes, and the strong effects may be related to the exotic nature of the cross. "The more genetically divergent the cross, the higher the power of the genome scan to detect something significant," says de Koning. Chinese and Dutch pigs have evolved independently for a relatively long period of evolutionary time, yet together they produce healthy piglets.

How molecular genetics could change conventional breeding

Genomic imprinting has generally been regarded as a rare phenomenon, but it may not be that rare after all. "It is intriguing and quite unexpected to find that imprinting seems to affect such a high percentage of traits of economic interest in pigs," says Michel Georges, of the Faculty of Veterinary Medicine at the University of Liege, Belgium. His laboratory is conducting whole-genome scans for imprinting in different pig crosses, and the pattern of recent discoveries makes him optimistic that the Dutch group's results will hold up.

Georges led the team that last year identified the imprinted chromosomal region called IGF2, which affects muscle and fat. Similar imprinted effects are present in corresponding regions of the human and mouse genomes. "The IGF2 region in the pig genome has been mapped in sufficient detail to compare with the analogous regions in mice and humans," says Georges. "It's clear that we're seeing imprinting effects that have been conserved throughout evolution."

The four regions reported by the Dutch group are relatively large sections of the genome and may contain thousands of genes. "We could be detecting the joint effect of a cluster of genes or the effect of a single gene," says de Koning. In humans and mice, most imprinted regions are arranged in chromosomal clusters. Although the evolutionary purpose of imprinting is largely a mystery, the effect has been linked to development, including fetal growth and brain development.

If imprinting influences muscular and fat development in pigs, then the laws of classical genetics would not apply to these traits. "Genes for these traits could not be manipulated without the breeders having knowledge of the imprinting effects," says Georges. "This is a very nice example of where molecular genetics has an edge over conventional breeding."

A purebred Meishan sow with her purebred offspring.

The power of molecular genetics in pig research was demonstrated ten years ago by the virtual elimination of the porcine stress gene. In 1990, researchers identified the gene, which is linked to anxiety and can result in sudden death when an animal is transported or put in an unfamiliar environment. Using a DNA test, pig producers were able to eliminate the gene from most breeding stock. The discovery led to the identification of a gene in humans that also can result in disease.

By understanding the mechanisms of imprinting, researchers could help breeders use a natural phenomenon to their advantage. As de Koning points out, the mother of piglets has requirements for energy reserves that her offspring do not. Knowing how genes governing body fat are inherited and expressed could allow breeders to derive specific mating combinations for the optimal animals.

Imprinted genes break the laws of classical genetics

Discovering the mechanisms of imprinting may take years, but laboratories around the world are now looking for the effect. "We have been testing for imprinting in all of our studies," says Gary Rohrer, a researcher at the US Meat Animal Research Center, Nebraska. "We are getting a lot of significant effects that are not due to traditional inheritance, some of which may involve imprinting." In January, Rohrer saw preliminary results of the Dutch study at the Plant & Animal Genome VIII Conference in California. Final results appeared in a recent issue of the Proceedings of the National Academy of Sciences.

The purpose of the paper, says de Koning, is to get researchers thinking about imprinting, and it seems to have done so. Georges at the University of Liege, for instance, is struck by the fact that imprinting may be a widespread phenomenon in the genome. "What is the biological meaning of this?" he asks. The answer to that question, he predicts, will have implications not only for livestock but also for human medicine.

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de Koning, D.-J. et al. Genome-wide scan for body composition in pigs reveals important role of imprinting. Proc Natl Acad Sci USA 97, 7947-7950 (July 5, 2000).

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