Accelerating genome-wide evolution through alternative chromosome configuration

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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 an atypical mode of chromosome arrangement on genome organization and evolution. Their findings are published in the journal cell.

In every single cell in our body, our DNA, the molecule that carries the instructions for development and growth, is packaged together with proteins into structures called chromosomes. Complete sets of chromosomes together make up the genome, all of an organism’s genetic information. In most organisms, including us, chromosomes appear as X-shaped structures when they are captured in their condensed and duplicated states in preparation for cell division. In fact, these structures may be among the most iconic in all of science. The X shape is due to a restricted region called the centromere that serves to connect sister chromatids, which are the identical copies formed by DNA replication of a chromosome. The most studied organisms are “monocentric”, that is, the centromeres are restricted to a single region of each chromosome. Several animal and plant organisms, however, show a very different centromere organization: instead of a solitary constriction as in classical X-shaped chromosomes, the chromosomes of these organisms harbor multiple centromeres that are arranged in a line from one end of a sister chromatid to the other. Thus, these chromosomes lack a primary constriction and are X-shaped, and species with these chromosomes are known as “holocentric,” from the ancient Greek word 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 surprising effects of this non-classical mode of chromosome organization on genome architecture and evolution.

To determine how holocentricity affects the genome, Marques and his team used highly accurate DNA sequencing technology to decode the genomes of three plants with grass-like flowers and closely related holocentric spikelets found around the world that are often the first conquerors of new habitats. For reference, the team also decoded the genome of its most closely related monocentric relative. Thus, comparing the edges of the holocentric beak with its monocentric relative allowed the authors to attribute the differences they observed to the effects of holocentricity.

Their analyzes reveal surprising differences in genome organization and chromosomal behavior in holocentric organisms. They found that centromere function is distributed among hundreds of small centromeric domains in holocentric chromosomes. Whereas in monocentric organisms, genes are largely concentrated away from centromeres and the regions immediately surrounding them, in holocentric species they are evenly distributed along the entire length of the chromosomes. In addition, in monocentric species chromosomes are known to mix with each other during cell division, a property that appears to play a role in the regulation of gene expression. In particular, these long-range interactions were sharply reduced at the edges of the bill with holocentromeres. Thus, holocentricity fundamentally affects the organization of the genome, as well as how chromosomes behave during cell division.

In holocentric organisms, almost any given chromosomal fragment will harbor a centromere and thus have adequate centromere function, which is not true for monocentric species. In this way, holocentromeres are thought to stabilize chromosomal fragments and fusions and thereby promote rapid genome evolution, or the ability of an organism to make rapid and wholesale changes to its DNA. In one of the beak edges they analyzed, Marques and his team were able to show that chromosome fusions facilitated by holocentromeres allowed this species to maintain the same number of chromosomes even after quadrupling the entire genome. In another of their analyzed beaks, a species with only two chromosomes, the lowest of any plant, holocentricity was found to be responsible for the dramatic reduction in chromosome number. Thus, holocentric chromosomes may enable the formation of novel 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, as well as allowing genomes to evolve rapidly through the fusion of their chromosomes.” 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 in the vicinity of 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 – more resistant and yielding crop species”.

SMC protein complex shown to ensure holocentromere dynamics More information: Paulo G. Hofstatter et al, Repeat-based holocentromeres influence genome architecture and karyotype evolution, cell (2022). DOI: 10.1016/j.cell.2022.06.045 Journal Information: Cell Provided by Max Planck Society

Citation: Accelerating genome-wide evolution using alternative chromosome configuration (2022, August 4) Retrieved August 4, 2022 from

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