A groundbreaking study challenges the existing knowledge about Genome stability in closely related organisms and offers new insights into the mechanisms behind extensive genome size variation.

Our current understanding of genomic stability and variability has been primarily shaped by a few model organisms, leaving the extent and universality of these findings uncertain. Despite the vast variation in genome size across the tree of life, with eukaryotes alone exhibiting a difference of over 200,000-fold, genome size has traditionally been considered stable within species or among closely related organisms.

However, a new study published in Genome Biology and Evolution by Takashi Tsuchimatsu, Yawako Kawaguchi, and their team from The University of Tokyo challenges this notion by uncovering significant variation in genome size among the Closterium peracerosum-strigosum-littorale (C. psl.) complex, a group of unicellular algae closely related to land plants.

Tsuchimatsu and Kawaguchi initially planned to perform standard population and comparative genomic analyses on 22 natural strains of the C. psl. complex. However, they were surprised to find that “the genomes of Closterium appeared to be much more complex than we had initially thought,” says Tsuchimatsu. The most exciting discovery was the extensive variation in genome size among morphologically indistinguishable algal strains.

The study revealed that the C. psl. strains exhibited a more than twofold variation in genome size, ranging from approximately 450 megabases to over 1,100 megabases. This finding prompted the researchers to redirect their focus towards investigating the factors underlying such substantial genome size variation.

By generating genome sequence data from six additional C. psl. strains with significantly different genome sizes, Tsuchimatsu and colleagues discovered that Copy Number Variation (CNV) across the entire genome, rather than duplication of specific chromosomes or proliferation of repeat sequences, plays a crucial role in driving the observed genome size dynamics in this species complex. CNVs occur when genes or large DNA segments are duplicated or deleted.

The researchers found that approximately 30% of genes exhibited variation in copy number, even among closely related C. psl. strains. This suggests that frequent duplications and deletions occurring throughout the genome contribute to the rapid changes in genome size.

Furthermore, the study revealed that gene expression levels did not increase proportionally with gene copy number for about 30% of the genes experiencing CNV. This indicates that an epigenetic process, like dosage compensation, maintains balanced gene expression despite changes in gene dosage.

By preserving extensive CNV and genome size variation within the C. psl. complex, dosage compensation helps mitigate the potential negative effects of changes in gene dosage. This sheds new light on the intricate relationship between gene copy number and expression levels and suggests that dosage compensation enables greater variation in genome size by increasing tolerance for CNVs.

These findings pave the way for further research into genome dynamics in this species complex and among microeukaryotes in general. According to Tsuchimatsu, “Although we found signatures of extensive segmental duplications, we do not yet have a clear map of how duplicate sequences are distributed across chromosomes. For this, it will be necessary to obtain chromosome-scale assemblies together with basic karyotype information, including chromosome numbers.”

However, observing chromosomes at a high resolution remains challenging in Closterium, presenting a major obstacle. Nonetheless, the research team has observed differences in chromosome numbers between C. psl. strains capable of mating with each other, suggesting a mechanism that tolerates chromosomal rearrangements during meiosis and providing a glimpse into additional genome dynamics in this species complex.

Further exploration of the C. psl. complex and other non-model species may continue to uncover the prevalence of such genome dynamics. A recent study by Piganeau and colleagues, also published in Genome Biology and Evolution, revealed a surprisingly high frequency of chromosomal duplications in experimental lines of unicellular green algae and provided evidence for dosage compensation at the chromosomal level.

By moving beyond observations in model organisms, these “exceptions” challenge the established rules of genomic stability and suggest that eukaryotic genomes are more dynamic than previously believed.

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