Three-dimensional Organization of Polytene Chromosomes in Somatic and Germline Tissues of Malaria Mosquitoes

Abstract

Spatial organization of chromosome territories and interactions between interphase chromosomes themselves, as well as with the nuclear periphery, play important roles in epigenetic regulation of the genome function. However, the interplay between inter-chromosomal contacts and chromosome-nuclear envelope attachments in an organism’s development is not well-understood. To address this question, we conducted microscopic analyses of the three-dimensional chromosome organization in malaria mosquitoes. We employed multi-colored oligonucleotide painting probes, spaced 1 Mb apart along the euchromatin, to quantitatively study chromosome territories in larval salivary gland cells and adult ovarian nurse cells of Anopheles gambiae, An. coluzzii, and An. merus. We found that the X chromosome territory has a significantly smaller volume and is more compact than the autosomal arm territories. The number of inter-chromosomal, and the percentage of the chromosome–nuclear envelope, contacts were conserved among the species within the same cell type. However, the percentage of chromosome regions located at the nuclear periphery was typically higher, while the number of inter-chromosomal contacts was lower, in salivary gland cells than in ovarian nurse cells. The inverse correlation was considerably stronger for the autosomes. Consistent with previous theoretical arguments, our data indicate that, at the genome-wide level, there is an inverse relationship between chromosome-nuclear envelope attachments and chromosome–chromosome interactions, which is a key feature of the cell type-specific nuclear architecture.

Reorganization of the nuclear architecture in the Drosophila melanogaster Lamin B mutant lacking the CaaX box

“…Interestingly, the level of heterochromatin underreplication is lower in ovarian pseudonurse cells than in salivary gland cells of D. melanogaster [46]. In agreement with this observation, the percentage of chromosome regions located at the nuclear periphery was typically higher in salivary gland cells than in ovarian nurse cells of mosquitoes [47]. Second, it has been shown that chromosomes occupy a significantly greater fraction of the nuclear volume in salivary glands (34%) than in other tissues with lower levels of polyteny [41].…”

Anophelesmosquitoes revealed new principles of 3D genome organization in insects

“…We hypothesized that the decrease of contact frequencies observed at large distances might be explained by the specific shape of chromosome territory. Indeed, it is known that chromosome territories are not spherical in mammalian 40,41 and mosquito 42 cells. If DNA occupies an ellipsoidal or cylindrical shape, then the radius of the cylinder will determine the characteristic spherical volume inside which the drop of contacts should be in agreement with the fractal globule model.…”

Chromatin Structure and Function in Mosquitoes

“…coluzzi, and An. merus) (George et al, 2020) found chromosome territories that appeared ellipsoidal in shape, not spherical, as in mammals (Khalil et al, 2007;Sehgal et al, 2014). This is important because these various shapes can influence the distance and frequencies of the spatial interactions in the genome (Lukyanchikova et al, 2020).…”

“…quinquefasciatus ( Naumenko et al, 2015 ), Cx. tarsalis ( Little, 2020 ), and several Anopheles species ( Cornel and Collins, 2000 ; Sharakhov et al, 2002 , 2004 , 2016 ; Sharakhova et al, 2010 ; George et al, 2010 , 2020 ; Xia et al, 2010 ; Jiang et al, 2014 ; Artemov et al, 2015 , 2017 , 2018 ; Neafsey et al, 2015 ; Wei et al, 2017 ; Lukyanchikova et al, 2020 ; Waterhouse et al, 2020 ), and they contributed not only to the improvement of the genomes annotation, by assessing the ordering and orientation of the contigs and scaffolds, but also to the study of the organization of centromeres in different cell types ( Sharakhova et al, 2019 ; Lukyanchikova et al, 2020 ). The advantage of these methods is that they make genome mapping more generalizable to non-model mosquitoes ( Sharakhova et al, 2019 ).…”

“… The regulatory genome of mosquitoes. (A) In Anopheles mosquitoes, as previously described for Drosophila ( Moretti et al, 2020 ), the attachment of the chromatin fiber to the nuclear envelope and lamina contributes to the organization and functional 3D structure of the genome, and it determines the contact frequencies between and within chromosomes ( George et al, 2020 ; Lukyanchikova et al, 2020 ). (B) The Rabl-like configuration described in Anopheles spp.…”