Tissue-Specific Differences in the Spatial Interposition of X-Chromosome and 3R Chromosome Regions in the Malaria Mosquito Anopheles messeae Fall.

Abstract

Spatial organization of a chromosome in a nucleus is very important in biology but many aspects of it are still generally unresolved. We focused on tissue-specific features of chromosome architecture in closely related malaria mosquitoes, which have essential inter-specific differences in polytene chromosome attachments in nurse cells. We showed that the region responsible for X-chromosome attachment interacts with nuclear lamina stronger in nurse cells, then in salivary glands cells in Anopheles messeae Fall. The inter-tissue differences were demonstrated more convincingly in an experiment of two distinct chromosomes interposition in the nucleus space of cells from four tissues. Microdissected DNA-probes from nurse cells X-chromosome (2BC) and 3R chromosomes (32D) attachment regions were hybridized with intact nuclei of nurse cells, salivary gland cells, follicle epithelium cells and imaginal disсs cells in 3D-FISH experiments. We showed that only salivary gland cells and follicle epithelium cells have no statistical differences in the interposition of 2BC and 32D. Generally, the X-chromosome and 3R chromosome are located closer to each other in cells of the somatic system in comparison with nurse cells on average. The imaginal disсs cell nuclei have an intermediate arrangement of chromosome interposition, similar to other somatic cells and nurse cells. In spite of species-specific chromosome attachments there are no differences in interposition of nurse cells chromosomes in An. messeae and An. atroparvus Thiel. Nurse cells have an unusual chromosome arrangement without a chromocenter, which could be due to the special mission of generative system cells in ontogenesis and evolution.

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

“…However, members of the An. maculipennis subgroup have the Rabl-like configuration in their salivary gland cells, but not in ovarian nurse cells in which chromosomes are more condensed, and heterochromatic regions of heterologous chromosomes are spatially separated at the nuclear periphery by as much as 120 • [32,104]. In non-polytene chromosomes of fruit flies, the contacts occurring between arms favor pairs belonging to the same chromosome [9].…”

Heterochromatin, histone modifications, and nuclear architecture in disease vectors

“…A very recent study applied chromosome region-specific microdissected paints to investigate tissue-specific features of chromosome architecture in An. messeae [43]. It found significant differences in the 3D interposition of the nuclear envelope attachment regions of the chromosomes X and 3R between somatic (salivary glands, follicle epithelium) and germ-line (ovarian of nurse cells) tissues, suggesting the link between the nuclear architecture and cell-type differentiation.…”

Tissue-specific features of the X chromosome and nucleolus spatial dynamics in a malaria mosquito, Anopheles atroparvus

“…Some lamin-associated domains (LADs) differ between cell types while others are common to different cell types in mammals [ 11 ]. Attachments of polytene chromosomes to the nuclear envelope (NE) occur via heterochromatic regions and have tissue-specific differences in Drosophila melanogaster [ 12 – 13 ] and in Anopheles mosquitoes from the Maculipennis group [ 14 – 16 ]. Studying spatial organization of CTs and nucleoli would be important for understanding the spatial organization of transcription inside the cell nucleus in malaria mosquitoes.…”

“…Knowledge about nuclear architecture in vectors of infectious diseases will provide a rich basis for fundamental and applied research aimed at deciphering the mechanisms controlling development and reproduction [ 17 ]. We have identified significant differences in interpositions of X and 3R chromosomes in several types of somatic and germ-line cells in Anopheles messeae [ 14 , 16 ]. On average, the X chromosome and 3R chromosome are located closer to each other in follicular epithelium cells (FE) in comparison with their location in ovarian nurse cells (NC).…”

“…On average, the X chromosome and 3R chromosome are located closer to each other in follicular epithelium cells (FE) in comparison with their location in ovarian nurse cells (NC). The imaginal disc cells nuclei have an intermediate arrangement of chromosome interposition, similar to that of other somatic cells and nurse cells [ 16 ].…”