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

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dc.contributor.authorWaters, P.D.
dc.contributor.authorPatel, H.R.
dc.contributor.authorRuiz-Herrera, A.
dc.contributor.authorÁlvarez-González, L.
dc.contributor.authorLister, N.C.
dc.contributor.authorSimakov, O.
dc.contributor.authorEzaz, T.
dc.contributor.authorKaur, P.
dc.contributor.authorFrere, C.
dc.contributor.authorGrutzner, F.
dc.contributor.authorGeorges, A.
dc.contributor.authorGraves, J.A.M.
dc.date.issued2021
dc.description.abstractMicrochromosomes, 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.
dc.description.statementofresponsibilityPaul D. Waters, Hardip R. Patel, Aurora Ruiz-Herrera, Lucía Álvarez-González, Nicholas C. Lister, Oleg Simakov, Tariq Ezaz, Parwinder Kaur, Celine Frere, Frank Grützner, Arthur Georges, and Jennifer A. Marshall Graves
dc.identifier.citationProceedings of the National Academy of Sciences of the United States of America, 2021; 118(45):e2112494118 -1-e2112494118 -11
dc.identifier.doi10.1073/pnas.2112494118
dc.identifier.issn0027-8424
dc.identifier.issn1091-6490
dc.identifier.orcidGrutzner, F. [0000-0002-3088-7314]
dc.identifier.urihttps://hdl.handle.net/2440/133811
dc.language.isoen
dc.publisherProceedings of the National Academy of Sciences
dc.relation.granthttp://purl.org/au-research/grants/arc/DP170101147
dc.relation.granthttp://purl.org/au-research/grants/arc/DP180100931
dc.relation.granthttp://purl.org/au-research/grants/arc/DP210103512
dc.relation.granthttp://purl.org/au-research/grants/arc/FT200100192
dc.rights© 2021 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
dc.source.urihttps://doi.org/10.1073/pnas.2112494118
dc.subjectVertebrate chromosome evolution; whole-genome alignment; chromosome conformation; microchromosome origin; amphioxus
dc.subject.meshAnimals
dc.subject.meshBase Sequence
dc.subject.meshBiological Evolution
dc.subject.meshChordata
dc.subject.meshChromosomes, Mammalian
dc.subject.meshConserved Sequence
dc.subject.meshGenome
dc.titleMicrochromosomes are building blocks of bird, reptile, and mammal chromosomes
dc.typeJournal article
pubs.publication-statusPublished

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