Aphid's genome reflects its reproductive, symbiotic lifestyle

The genome of the pea aphid, sequenced by the International Aphid Genomics Consortium, reflects these unusual characteristics and more, said Dr. Stephen Richards, assistant professor in the Baylor College of Medicine Human Genome Sequencing Center and leader of the sequencing effort. The consortium released the 464 megabyte draft genome of the pea aphid (Acyrthosiphon pisum) in the current issue of PLoS Biology.

"Because this is a different kind of insect -- not a fruit fly, not a beetle ... -- we are seeing things that people have not seen in other projects," Richards said.

Dr. David Stern, professor of ecology and evolutionary biology at Princeton University, said that even though he pushed hard to get the aphid genome sequenced, "it turned out to be far more interesting than I was expecting."

He agreed with Richards that the aphid presents a special case.

"Look at this little insect, sitting on a plant and sucking plant juices. You don't realize that it is involved in a historic battle with plants for access to its life blood. All its genes have evolved to allow it to exploit its feeding relationship," said Stern.

"We found a lot of genes -- 35,000 compared to 15,000 to 20,000 in other insects and 25,000 in humans," said Richards, a corresponding author of the paper.

"Thus it seems that pea aphids (one among the 4,500 other aphid species on the planet) have duplicated some of their genes," said Dr. Denis Tagu, senior scientist with the French National Institute for Agricultural Research. "What does this mean? It means that the pea aphid probably did a kind of 'back-up' of its genetic material. One hypothesis is that one copy of this back-up is kept unchanged and used for the functioning of the cells and the organism, and that the second set can allow modifications by mutations."

"Most of the mutations are probably neutral or negative for the genes, with no effect on the biology of the organism. But some rare mutations might produce new functions for some of the genes that might help, in this case, the pea aphid adapt to its environment."

"Another possibility is that maybe aphids require extra copies of genes because they have such complex life cycles," Stern said.

"They have multiple forms to adapt to different environments. There are winged forms, forms without wings. Some produce asexually but give birth to life offspring. When the environment becomes more hostile, as in the fall, they give birth to males whose only purpose is to mate with females, who then lay eggs that hatch later on," Stern said.

"Maybe the aphids need all these to regulate all parts of their life cycles. This genome has generated far more exciting questions than we could have anticipated. There is more mystery in this genome than anyone would have expected," he said.

"The fact that they can reproduce both sexually and asexually makes them a useful system for understanding genome evolution in sexual versus asexual reproduction," said Dr. Alex Wilson, assistant professor of evolutionary biology at the University of Miami. In addition, she said, because the genome of the symbiotic Buchnera aphidicola was sequenced 10 years ago, this is the first system in which scientists can look at both the genomes of the host and its bacterial symbiote.

"This genomic discovery opens new roads to understanding the adaptive processes of these animals to adverse conditions," Tagu said.

Richards agreed. "It is interesting because of this polyphenism (multiple phenotypes or observable characteristics arising from the same genotype). Is this one and one-half gene sets? If so, how do you regulate the extra genes?"

"When I first started working on them, I thought of them as little tiny cows," said Dr. Nicole Gerardo, assistant professor at Emory University in Atlanta. As she began to explore their role as agricultural pests further, the relationship between the insect and its symbiotic bacteria Buchnera became more interesting.

"Aphids seem to be missing many of these genes that are important to immune response," she said. "Our preliminary research suggested aphids might have a weak immune system. That was biologically interesting. What would lead to loss of the immune system?"

The Buchnera have become machines for producing amino acids lacking in the aphid.

"We are interested in exploring the aphid immune response and how it relates to protective bacteria. If you have protective bacteria, do you need to invest in an immune response?" she said.

"Aphids and Buchnera have become the central model for a kind of highly specialized animal-bacterial symbiosis in which the bacteria occur within the cytosol (the watery interior) of specialized host cells and are inherited from the mothers," said Dr. Nancy Moran, professor of ecology and evolutionary biology at the University of Arizona in Tucson.

During the millions of years that these two symbiotes have evolved, the Buchnera genome has shrunk to no more than 15 percent of its original size, but it retains a full complement of genes for production of essential amino acids, said Moran.

"These amino acids are the raison d'etre of the symbiosis because the aphid diet lacks these required nutrients and the insects cannot make their own," she said.

Tagu said that sequencing the genome may give scientists tools they can use to control pests such as aphids.

"It is similar to describing the anatomy of the human body, in the past. We are at the very beginning of using it to understand how these insects function and how they are adapted to feed from plants and provoke damage in agriculture. Understanding the molecular dialogue between bacterial and aphid genes could lead to discovery of key regulatory mechanisms that can decrease the efficiency of the symbiosis and disrupt the aphid's impact on crops."

Many more papers generated by this project are appearing in a special issue of the journal Insect Molecular Biology (http://www3.interscience.wiley.com/journal/118497253/home) .

Richards and Dr. Richard A. Gibbs of BCM headed the sequencing project. Project leaders included Gerardo, Moran, Richards, Stern, Tagu, Wilson and Dr. Atsushi Nakabachi of the Advanced Science Institute in Japan. Scientists from more than 10 nations took part in the sequencing and analysis of the genome.