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Microchromosomes are building blocks of bird, reptile, and mammal chromosomes
Journal article   Peer reviewed

Microchromosomes are building blocks of bird, reptile, and mammal chromosomes

Paul D Waters, Hardip R Patel, Aurora Ruiz-Herrera, Lucía Álvarez-González, Nicholas C Lister, Oleg Simakov, Tariq Ezaz, Parwinder Kaur, Celine Frere, Frank Grützner, …
National Academy of Sciences. Proceedings, Vol.118(45), pp.1-11
2021
PMCID: PMC8609325
PMID: 34725164
url
https://doi.org/10.1073/pnas.2112494118View
Published Version

Abstract

vertebrate chromosome evolution whole-genome alignment chromosome conformation microchromosome origin amphioxus
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 comparisons, 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 microchromosomes, 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 spatially separated into a central compartment at interphase and during 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 microchromosomes 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 microchromosomes, 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 elements, represent fundamental building blocks of amniote chromosomes, and it is mammals, rather than reptiles and birds, that are atypical.

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