Microchromosomes are building blocks of bird, reptile and mammal chromosomes

Abstract

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, that are atypical.

Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

“…The high global stability of macro-and microchromosomes between sea turtle families also aligns with recent work showing similar patterns across reptiles, including birds, emphasizing the important roles of microchromosomes in vertebrate evolution (55). Higher evolutionary rates for microchromosomes relative to macrochromosomes has been documented in intraspecific (56) and interspecific (57) studies with chicken and turkey genomes, respectively, so it is possible that the characteristics of microchromosomes and RRCs we observed are not unique to sea turtles, but rather, are prevalent in many vertebrates, which will become clearer as more high-quality assemblies are produced.…”

A phased chromosome-level genome and full mitochondrial sequence for the dikaryotic myrtle rust pathogen, Austropuccinia psidii

“…Genome-wide synteny analysis of chromosome-level assemblies can be extremely useful for identifying possible scaffolding errors in phased haploid genomes (Figure 2A) or investigating chromosome evolution across species (Waters et al 2021). Full genome alignments are computationally intensive, especially for species that are rich with repetitive sequences, such as A. psidii.…”

Linked-Read Sequencing of Eight Falcons Reveals a Unique Genomic Architecture in Flux

“…Microchromosomes may also contain a higher density of structural variants ( Völker et al 2010 ), a lower density of repetitive elements ( International Chicken Genome Sequencing Consortium 2004 ), and higher levels of interchromosomal chromatin ( trans- ) associations ( Lui et al 2021 ). Debate continues as to whether the special characteristics of microchromosomes are a product of their size or a product of their sequence motifs ( O’Connor et al 2019 ; Waters et al 2021 ). The fusions of microchromosomes in falcons provide an opportunity to assess this.…”

“…Generally, birds appear to be close to AT–GC equilibrium in overall genome-wide base composition with high-GC isochores concentrated on microchromosomes ( Mugal et al 2013 ; Costantini and Musto 2017 ), and ongoing expansion of genomic heterogeneity such that high-GC regions continue to gain GC content and low GC regions continue to lose it ( Webster et al 2006 ). Mammals, in contrast, lost their microchomosomes in a common ancestor more than 200 Ma and are losing GC content from high-GC isochores ( Duret et al 2002 ; Waters et al 2021 ) and moving toward greater genomic homogeneity in several lineages. The biased-gene-conversion hypothesis (BGCH) provides an explanation for these observations and proposes that high-GC isochores formed and are maintained by high recombination rates, which favor conversion and fixation of AT-to-GC substitutions.…”

“…Biased gene conversion and CpG hypermutability are also well documented in birds ( Webster et al 2006 ; Mugal et al 2015 ), as in other amniotes ( Figuet et al 2015 ), and make contrasting contributions to patterns of AT–GC equilibrium across avian genomes ( Weber et al 2014 ). However, due to high levels of correlation in the genomic features of birds with chromosome type ( Mugal et al 2013 ; Kawakami et al 2017 ), the relative roles of chromosome type and similarity in sequence motifs are difficult to disentangle ( Waters et al 2021 ). Localized chromosomal rearrangements have, however, been shown to alter substitutional biases in a manner consistent with the BGCH in mammals and birds ( Auton et al 2012 ; Mugal et al 2013 ).…”