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Solving the Centromere Paradox

Corn chromosomes contain vastly different amounts of tandem repeat CenC (green fluorescence) at their centromeres as illustrated by this HI47 karyotype. The ten maize chromosomes are lined up to the stippled white line at their centromeres. (Image courtesy of Albert and Birchler)

By Shelley Littin, CyVerse, and Frederika Bain, University of Hawai'i

Researchers tapped publicly accessible data in CyVerse to solve the longstanding Centromere Paradox. Their work is published in the Proceedings of the National Academy of Sciences.

“The importance of centromeres in cell division” drove University of Hawai’i geneticist Gernot Presting and his team to take on the study of centromeres.

On the X-shaped chromosome, the centromere is at the “cross” point of the two arms. Like the rest of the chromosome, centromeres are composed of double-stranded DNA and protein. Centromeres play an essential role in cell division by ensuring that each new cell obtains a complete set of chromosomes.

Because the centromeres of all organisms play the same role, it seems logical that an optimal DNA sequence might have evolved to perform this function, and that all centromeres would have the same sequence. However, centromere DNA is highly variable. Worse yet for research purposes, it tends to consist of repetitive sequences that are difficult to study.

This phenomenon has been called the Centromere Paradox, and scientists have been trying to figure out what causes it. A previously proposed solution, the centromere drive hypothesis, suggests that an evolutionary “arms race” between centromeric DNA and its binding proteins necessitates their rapid evolution, has yet to be proven conclusively.

Presting’s team studied turnover of DNA in centromeres of corn, because of the vast amount of genetic data available for corn and because of its importance as a food crop.

“Although corn was domesticated 10,000 years ago and can interbreed with its wild relatives, all corn contains, a single centromere version on three of its chromosomes, so there must be something linked to those centromeres that is selected for very vigorously in cultivated corn” Presting said.

Kevin Schneider and Thomas Wolfgruber are members of Presting's research team. (Image: University of Hawai'i at Manoa, CTAHR)

Kevin Schneider and Thomas Wolfgruber are members of Presting's research team. (Image: University of Hawai'i at Manoa, CTAHR)

The team downloaded publicly accessible data on maize genomes from CyVerse, a National Science Foundation-funded project to connect researchers around the world by providing the computational infrastructure for managing large datasets, and sharing data, analyses, and results with collaborators.

Delving through the data, the researchers discovered an alternative explanation for the Centromere Paradox, offering a major advance in the understanding of centromere evolution.

“We showed that there are a lot of chromosomal inversions near centromeres, bringing genes near centromeres. Previously it was thought that centromere DNA sequences themselves are subject to evolution, instead of these genes,” Presting explained. “Researchers have not considered that selection for genes in centromeres might affect the repetitive DNA sequences making up centromeres.”

“It appears that the turnover of DNA in corn centromeres over the past 10,000 years is linked to the presence of these agronomically important genes in the centromere.”

The finding emphasizes a longstanding genetic problem for breeders, Presting said. “There’s no genetic recombination in centromeres, so all the recombination happens in the chromosome arm. This means that genes with important domestication or agronomic phenotypes that lie near centromeres will remain inextricably linked to that centromere.”

Presting hopes that his team’s findings will give a new direction for researchers to investigate.  “There’s evidence now that intensive breeding is a big factor in centromere evolution,” he said.

Perhaps with greater knowledge about centromeres, breeders will be able to relocate centromeres on chromosomes or use artificial chromosomes with functioning centromeres to select for desired plant traits, Presting said.

Following their study, Presting’s team deposited their supplementary data into CyVerse’s Data Store, making it available for future research teams. A member of Presting’s team also used CyVerse’s freely available tools for genetic analysis to resequence one of the corn centromeres for another research publication.

The team worked with a consortium of researchers studying plant centromeres, including Kelly Dawe at the University of Georgia, Jiming Jiang at the University of Wisconsin, James Birchler at the University of Missouri, and Jeffrey Ross-Ibarra at University of California, Davis. Their work was funded by the National Science Foundation, the United States Department of Agriculture, and the University of Hawai’i.