Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 118, Issue 45, Pages -Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2112494118
Keywords
vertebrate chromosome evolution; whole-genome alignment; chromosome conformation; microchromosome origin; amphioxus
Categories
Funding
- Pawsey Supercomputing Centre
- Australian Government
- Government of Western Australia
- Australian Research Council [DP170101147, DP180100931, DP210103512, FT200100192]
- Australian National University research fellowship
- Spanish Ministry of Economy and Competitiveness [CGL2017-83802-P]
- Spanish Ministry of Science and Innovation [PID2020-112557GB-I00]
- FPI predoctoral fellowship from the Spanish Ministry of Economy and Competitiveness [PRE-2018-083257]
- Australian Research Council [FT200100192] Funding Source: Australian Research Council
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The study found that microchromosomes, as elements of an ancient animal genome, are highly conserved in birds and share synteny with certain small chromosomes in the chordate amphioxus. Turtles and squamates have independently lost microchromosomes through fusion events, resulting in different fusion patterns in different lineages. Microchromosomes are spatially separated into a central compartment in cells, showing higher interaction between microchromosomes compared to macrochromosomes.
Microchromosomes, once considered unimportant shreds of the chicken genome, are gene-rich elements with a high GC content and few transposable elements. Their origin has been debated for decades. We used cytological and whole-genome sequence com-parisons, and chromosome conformation capture, to trace their origin and fate in genomes of reptiles, birds, and mammals. We find that microchromosomes as well as macrochromosomes are highly conserved across birds and share synteny with single small chromosomes of the chordate amphioxus, attesting to their origin as elements of an ancient animal genome. Turtles and squamates (snakes and lizards) share different subsets of ancestral microchro-mosomes, having independently lost microchromosomes by fusion with other microchromosomes or macrochromosomes. Patterns of fusions were quite different in different lineages. Cytological observations show that microchromosomes in all lineages are spa-tially separated into a central compartment at interphase and dur-ing mitosis and meiosis. This reflects higher interaction between microchromosomes than with macrochromosomes, as observed by chromosome conformation capture, and suggests some functional coherence. In highly rearranged genomes fused microchromo-somes retain most ancestral characteristics, but these may erode over evolutionary time; surprisingly, de novo microchromosomes have rapidly adopted high interaction. Some chromosomes of early-branching monotreme mammals align to several bird micro -chromosomes, suggesting multiple microchromosome fusions in a mammalian ancestor. Subsequently, multiple rearrangements fueled the extraordinary karyotypic diversity of therian mammals. Thus, microchromosomes, far from being aberrant genetic ele-ments, represent fundamental building blocks of amniote chromo-somes, and it is mammals, rather than reptiles and birds, that are atypical.
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