Anopheles mosquitoes reveal new principles of 3D genome organization in insects

Abstract

Chromosomes are hierarchically folded within cell nuclei into territories, domains and subdomains, but the functional importance and evolutionary dynamics of these hierarchies are poorly defined. Here, we comprehensively profile genome organizations of five Anopheles mosquito species and show how different levels of chromatin architecture influence each other. Patterns observed on Hi-C maps are associated with known cytological structures, epigenetic profiles, and gene expression levels. Evolutionary analysis reveals conservation of chromatin architecture within synteny blocks for tens of millions of years and enrichment of synteny breakpoints in regions with increased genomic insulation. However, in-depth analysis shows a confounding effect of gene density on both insulation and distribution of synteny breakpoints, suggesting limited causal relationship between breakpoints and regions with increased genomic insulation. At the level of individual loci, we identify specific, extremely long-ranged looping interactions, conserved for ~100 million years. We demonstrate that the mechanisms underlying these looping contacts differ from previously described Polycomb-dependent interactions and clustering of active chromatin.

Strong interactions between highly dynamic lamina-associated domains and the nuclear envelope stabilize the 3D architecture of Drosophila interphase chromatin

“…Also, the strength of TAD-TAD interactions can naturally vary during life of organisms. For example, the chromatin compartmentalization is weaker in embryonic cells and stronger in adult cells of Anopheles mosquitoes [64]. Given that attractive TAD-TAD interactions play a major role in compartmentalization, will the global chromatin architecture, such as its radial distribution, become more sensitive or less sensitive to the variations in these interactions upon lamin depletion?…”

Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae)

“…2 a). We postulate that this non-random genomic distribution of synteny breaks is causally connected to their more open chromatin state (A compartments) and perhaps to a resulting higher chromatin fragility (relative to B compartments), as in animal species [ 28 , 48 ].

Fig.

…”

“…Genomic rearrangements occurring during evolution may have functional and hence evolutionary consequences arising from 3D chromatin architectural changes. Recent studies in animal species have explored the impacts of rearrangements on 3D chromatin architecture accompanying chromosome evolution [ 5 – 8 , 26 – 28 , 61 ]. These evolutionary dynamics are underexplored in plants, with little understanding of the higher-order outcomes of rearrangements with respect to hierarchical chromatin architectural features and gene expression.…”

“…S14). Several possible scenarios could explain how epigenetic modifications promote chromosomal breaks and associated rearrangements, including ( i ) relatively open chromatin regions might facilitate genomic rearrangements by increasing local chromatin fragility [ 28 , 48 , 64 ]; ( ii ) uncharacterized epigenetic-sensitive protein factors binding to chromatin might be involved in genomic rearrangements; and ( iii ) chromatin regions with common epigenetic states could preferentially interact, facilitating rearrangements. Insights into the relevance of these speculations will likely require both a new understanding of the molecular biology of epigenetics and recombination, along with an additional study of a diversity of species that encompass a wide range of genomic features and rearrangements.…”

“…Available studies in animal and several plant models have implicated preferential occurrence of synteny breaks associated with particular chromatin architectural features. Within mosquitoes, synteny breaks preferentially occurred within active euchromatic regions belonging to A compartments [ 28 ]. At a finer scale, the co-localization of synteny breaks with TAD boundaries has been consistently identified in chicken, gibbon, fruit fly, and green pepper [ 5 – 7 , 26 ].…”