3D organization of chicken genome demonstrates evolutionary conservation of topologically associated domains and highlights unique architecture of erythrocytes’ chromatin

Abstract

How chromosomes are folded, spatially organized and regulated in three dimensions inside the cell nucleus are among the longest standing questions in cell biology. Genome-wide chromosome conformation capture (Hi-C) technique allowed identifying and characterizing spatial chromatin compartments in several mammalian species. Here, we present the first genome-wide analysis of chromatin interactions in chicken embryonic fibroblasts (CEF) and adult erythrocytes. We showed that genome of CEF is partitioned into topologically associated domains (TADs), distributed in accordance with gene density, transcriptional activity and CTCF-binding sites. In contrast to mammals, where all examined somatic cell types display relatively similar spatial organization of genome, chicken erythrocytes strongly differ from fibroblasts, showing pronounced A- and B- compartments, absence of typical TADs and formation of long-range chromatin interactions previously observed on mitotic chromosomes. Comparing mammalian and chicken genome architectures, we provide evidence highlighting evolutionary role of chicken TADs and their significance in genome activity and regulation.

Topologically associating domains and their role in the evolution of genome structure and function inDrosophila

“…melanogaster TADs are highly conserved across cell types, tissues and species (Dixon et al 2012;Vietri Rudan et al 2015;Fishman et al 2019) . To investigate conservation of this spatial structure during Drosophila evolution, we compared TADs between D. pseudoobscura and D. melanogaster , which diverged about ~49 million years ago (Thomas and Hahn 2017) .…”

“…Conservation of TAD structures between the two distantly related Drosophila species further prompted us to ask if disruption of TAD integrity (i.e. TAD shuffling or fusing as a result of large-scale chromosomal arrangements) in Drosophila is also constrained during evolution as previously shown in other animals such as mammals (Krefting et al 2018;Lazar et al 2018) and birds (Fishman et al 2019) . We test this by analyzing the distribution of chromosomal rearrangement breakpoints (using synteny breaks as the proxy) along the TAD body.…”

“…Topologically associating domain (TADs), one of these organizational features, was originally discovered in Hi-C contact maps as domains within which DNA sequences physically contact each other more densely than they are outside (Sexton et al 2012;Dixon et al 2012) . TADs or similar domains have been widely observed across the kingdom of life, from yeast (Mizuguchi et al 2014) and bacteria (Le et al 2013) to plants (Liu et al 2017;Xie et al 2019) and animals (Fishman et al 2019) .…”

Anophelesmosquitoes revealed new principles of 3D genome organization in insects

“…Comparative studies performed on multiple vertebrate species revealed that genome architecture is evolutionarily conserved and could be explained by dynamic interplay between processes of cohesin-mediated loop extrusion and chromatin compartmentalization [5][6][7][8] . In insects, comprehensive analyses [9][10][11][12][13] and cross-species comparisons 12,14 of genome architecture have to date focused only on Drosophila species.…”

Reorganisation of chromatin during erythroid differentiation

“…В нашей лаборатории получены данные о том, что при полной остановке транскрипции в эритроцитах курицы ядро действительно переходит в равновесное состояние: данные, полученные при помощи HiC и электронной микроскопии, говорят о максимально выраженной сегрегации компартментов активного и неактивного хроматина. При этом полученные карты хроматиновых взаимодействий свидетельствуют о полном отсутствии ТАДов и петель (Fishman et al, 2019). Исчезновение регуляторных петлевых взаимодействий не может быть объяснено остановкой транскрипционной активности и, соответственно, продвижения комплекса ассоциированных с транскрипцией белков, поскольку в ядрах сперматозоидов, также транскрипционно неактивных, доменная организация сохранялась.…”