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November 1996

Scientists identify retrovirus-like components in corn genome

WEST LAFAYETTE, Ind. -- Scientists have long known that genes make up only a tiny percent of the genetic material in a cell, but the question remained, "What are all those other things?"

A Purdue University study of the corn plant is fielding this question and producing some surprising kernels of knowledge about the organization and makeup of genetic material in plants. The findings offer new insights into why some plants have larger genomes than others, and they indicate that some plants may be able to thwart certain viruses that are devastating to humans.

Every living organism has a genome, the DNA in each cell's nucleus, which includes the active genes that determine the organism's characteristics. However, the genome also contains inactive pieces of DNA and other materials, many of which had not been identified.

In the Nov. 1 issue of the journal Science, Purdue biologist Jeffrey Bennetzen reports that the maize genome consists primarily of a class of mobile DNA called retrotransposons. Though these segments of DNA are not part of the active genes in the corn plant, they have the ability to multiply, move about and insert themselves throughout the genome.

"We knew that this mobile DNA was present to some extent in all genomes, including humans, but we didn't realize it could make up such a huge part of it," Bennetzen says. "Our study indicates that, in maize, mobile DNA accounts for more than 60 percent of the genome, which is two to three times more than what we would have expected to find."

Though scientists don't know how or why such segments of DNA accumulate in the genome, the fragments are thought to be generally harmless, Bennetzen says.

In the study, Bennetzen's group analyzed a region of the maize genome that contained two genes. The group discovered 10 different classes of retrotransposons within the region, with each class having 10 to 30,000 copies of its DNA segments scattered throughout the rest of the genome.

In addition to finding greater numbers of mobile DNA segments than expected, the Purdue team discovered that the retrotransposons organize themselves in a unique manner, inserting themselves within each other like nesting dolls, and burrowing between genes rather than inserting into the genes, as expected.

"We don't know how they do this, but because they target their insertions between genes, these repetitive elements have managed to side-step some very negative effects on their host," Bennetzen says. "For example, if these elements were inserted into genes in such a way as to cause mutations, you could wind up with more than 30,000 mutations per individual plant, and a dead host."

Instead, the retrotransposons insert themselves in positions where they tend to be inactive, allowing them to sit quietly and not drain energy from the host, he says. The result is that the mobile DNAs "hide" within the genome, where they can be passively transmitted to the next plant generation.

"These 'selfish DNAs,' as they're sometimes called, can hitchhike on the host DNA replication system because higher organisms apparently don't have a good system for getting rid of DNA once it gets into their genome," Bennetzen says. "In this way, they can replicate, and thereby survive into the next generation, even if the host doesn't want them."

Because this type of DNA is present and highly repeated in many species, Bennetzen says such elements may account for a large percentage of genetic material in other plants and animals with large genomes.

"The question we now have is 'How do those plants with small genomes, such as rice, restrain these prolific DNA segments?'" he says.

The study also indicates that many of these retrotransposons in corn appear to be retrovirus-like parasites, an unexpected finding because other organisms with such matter in their genomes, such as humans, are susceptible to retroviral diseases. Active retroviruses have never been seen in plants.

"Despite the fact that more than half its genome consists of this retrovirus-like DNA, corn is not known to have any retroviral diseases," Bennetzen says. "If these retrovirus agents are there, but don't succeed in making the plants sick, there's a possibility that maize has developed a mechanism to defeat them in some way."

His group now is initiating studies to determine whether any of these mobile DNA segments are in fact fragments of infectious retroviruses. If so, the scientists will begin analyzing how the corn plants may have worked to prevent the retroviruses from causing disease.

"If such a mechanism exists, scientists may be able to apply it to help animals and humans fight retroviruses, which cause a number of devastating illnesses such as some forms of cancer and AIDS," Bennetzen says.

The group also is trying to answer other questions raised by the findings, such as where the mobile DNA segments come from and how they get into the genome, and how the retrotransposons find their target sites between genes.

Bennetzen's group at Purdue worked with Keith J. Edwards of the Long Ashton Research Station in England. The research was funded by the U.S. Department of Agriculture.

smg/bennetzen.genes/9610f55

Source: Jeffrey Bennetzen, (765) 494-4763; e-mail., maize@bilbo.bio.purdue.edu

Writer: Susan Gaidos, (765) 494-2081; e-mail, susan_gaidos@purdue.edu

ABSTRACT

Nested retrotransposons in the intergenic regions of the maize genome

Phillip SanMiguel, Alexander Tikhonov, Young-Kwan Jin, Natasha Motchoulskaia, Dmitrii Zakharov, Admasu Melake-Berhan, Patricia S. Springer, Keith J. Edwards, Michael Lee, Zoya Avramova, and Jeffrey L. Bennetzen

The relative organization of genes and repetitive DNAs in complex eukaryotic genomes is not well understood. Diagnostic sequencing indicated that a 280 kb region containing the maize Adhl-F and u22 genes is composed primarily of retrotransposons inserted within each other. Ten retroelement families were discovered, with reiteration frequencies ranging from 10 copies to 30,000 copies per haploid genome. These retrotransposons accounted for over 60% of the Adhl-F region and at least 50% of the nuclear DNA of maize. These elements were largely intact and are dispersed throughout the gene-containing regions of the maize genome.


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