Accelerating evolution at the genome level through an alternative configuration of chromosomes

A research team led by André Marques at the Max Planck Institute for Plant Breeding Research in Cologne, Germany, has discovered the profound effects of a atypical manner of chromosomal arrangement on genome organization and evolution. Their findings are published in the journal Mobile.

In each individual cell of our body, our DNA, the molecule carrying the guidelines for the development and growth, is packed with proteins into constructs called chromosomes. Complete sets of chromosomes together make up the genome, the entire genetic information of an organism. In most organisms, including us, chromosomes appear as X-shaped constructs when captured in their condensed and duplicated states in preparation for cell division. Indeed, these constructs may be among the most iconic in all of science. The X-shape is due to a constricted region called the centromere which serves to connect sister chromatids, which are the identical copies formed by DNA replication of a chromosome. Most of the organisms studied are “monocentric”, which means that the centromeres are restricted to a single region on each chromosome. However, several animal and plant organisms show a very different centromere organization: instead of a solitary constriction as in the classic X-shaped chromosomes, the chromosomes of these organisms harbor several centromeres which are arranged in a line from one end to one sister chromatid to the other. Thus, these chromosomes do not have a primary constriction or an X-shape, and species with such chromosomes are called “holocentric”, from the ancient Greek hólos meaning “whole”.

A new study led by André Marques of the Max Planck Institute for Plant Breeding Research in Cologne, Germany, now reveals the striking effects of this unconventional mode of chromosome organization on the architecture and evolution of the genome.

To determine how holocentricity affects the genome, Marques and his team used highly precise DNA sequencing technology to decode the genomes of three sedges at closely related holocentric beak, grass-like flowering plants found throughout the world and often the first conquerors of new habitats. For reference, the team also decoded the genome of their most closely related monocentric dad or mum. Thus, comparing holocentric beaked sedges with their monocentric parent allowed the authors to attribute any observed difference to holocentricity effects.

Their analyzes reveal striking differences in genome organization and chromosome behavior in holocentric organisms. They found that centromere function is distributed across hundreds of small centromere domains in holocentric chromosomes. Whereas in monocentric organisms the genes are largely concentrated away from the centromeres and the regions immediately surrounding them, in holocentric species they are evenly distributed throughout the length of the chromosomes. Furthermore, in monocentric species, chromosomes are known to engage in a high degree of entanglement with each other during cell division, a property that appears to play a role in regulating the expression of Genoa. Notably, these long-range interactions were strongly diminished in beaked sedges with holocentromeres. Thus, holocentricity fundamentally affects the organization of the genome as well as the behavior of chromosomes during cell division.

In holocentric organisms, almost any given chromosomal fragment will house a centromere and therefore have proper centromere function, which is not true for monocentric species. In this way, holocentromeres are thought to stabilize chromosomal fragments and fusions and thus promote rapid genome evolution, or the ability of an organism to make rapid, global changes to its DNA. In one of the beaked sedges they analyzed, Marques and his team were able to show that holocentromere-mediated chromosome fusions allowed this species to retain the same number of chromosomes even after the entire genome quadrupled. In another of their analyzed beaked sedges, a species with only two chromosomes, the lowest of all plants, holocentricity was found to be responsible for the dramatic reduction in chromosome number. Thus, holocentric chromosomes could enable the formation of new species through rapid evolution at the genome level.

According to Marques, “Our study shows that the transition to holocentricity has greatly influenced the way genomes are organized and regulated, while allowing genomes to evolve rapidly by fusing their chromosomes together.” The team’s findings also show exciting implications for plant breeding, which typically relies on the ability to exchange DNA and genes between chromosomes and organisms. “Holocentric plants allow DNA exchange near centromeres, which is normally suppressed in monocentric species. Understanding how holocentrics do this could allow us to ‘unlock’ these genes in monocentric species and make them accessible for the breeding of better-performing and more resilient plant species.

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