Evolutionary Genomics: The Genes for Antifreeze Proteins Are Descended from Genes for Other Functional Proteins

Among the antifreeze proteins (AFPs) in polar fish, there are several known major types that are independently evolved. How did they evolve? What were their evolutionary precursors?

One type of AFP is indirectly evolved from a digestive enzyme protein! This astounding insight comes from genomic studies of the Antarctic toothfish (see Figure 10.19A). By means of gene sequencing, researchers recognized similarities in the gene that codes for the AFP and the gene that codes for a trypsin-like digestive enzyme secreted by the pancreas (see pages 155–156). Then, exploring the genome of the toothfish, they found an unusual gene: a single gene that encompasses the genetic code for both the digestive protein and the AFP. This gene demonstrates and illustrates how the original gene for the trypsin protein could have evolved into the gene that codes for the AFP. In fish that produce this particular type of AFP, most of the AFP is synthesized in the stomach and pancreas, and secreted into the gut lumen. Only later does it enter the blood. This strange path to the blood reinforces the conclusion that the gene for the AFP is descended from the digestive trypsin gene.

In 2010, the evolutionary origin of a second type of AFP was discovered, and this evolutionary scenario turns out to be amazingly parallel. Sialic acid is an important cytosolic compound. Through studies based on gene sequencing and controlled gene expression, researchers discovered in an Antartic fish (see the figure) a sialic-acid synthesis gene that also includes the code for a protein with rudimentary antifreeze properties. They then established that this gene duplicated during evolution. Whereas one copy continued its prior role, the other ceased to be involved in that role and instead evolved into a gene coding for a highly effective AFP.

A fish that provides insight into gene evolution  A gene found in the genome of the Antarctic eelpout (Lycodichthys dearborni) probably evolved to have a rudimentary antifreeze function in addition to its traditional function. After duplication of the gene, one copy evolved to code for one of the major types of AFPs in Antarctic fish. (Courtesy of Christina Cheng.)

Based on these cases, it appears that when polar fish first confronted the threat of freezing, variants of old protein-synthesizing genes underwent evolution to produce new genes specialized for synthesis of proteins with antifreeze properties. This discovery reminds us of François Jacob’s “tinkering” model for evolution (see page 10). Jacob emphasized that evolution makes new things from old, preexisting things, rather than starting from scratch. In the case of the AFPs discussed here, the gene for one was made from a gene for a digestive enzyme, and the gene for the other was made from a gene for cytosolic sialic-acid synthesis. Box Extension 10.2 provides references that will enable you to learn more about these fascinating genomic insights.

References

Cheng, C.-H. C., and L. Chen. 1999. Evolution of an antifreeze glycoprotein. Nature 401: 443–444.

Deng, C., C.-H. C. Cheng, H. Ye, X. He, and L. Chen. 2010. Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc. Natl. Acad. Sci. U.S.A 107: 21593–21598.

Duman, J. G. 2015. Animal ice-binding (antifreeze) proteins and glycolipids: an overview with emphasis on physiological function. J. Exp. Biol. 218: 1846–1855.