TY - JOUR

T1 - Anopheles mosquitoes reveal new principles of 3D genome organization in insects

AU - Lukyanchikova, Varvara

AU - Nuriddinov, Miroslav

AU - Belokopytova, Polina

AU - Taskina, Alena

AU - Liang, Jiangtao

AU - Reijnders, Maarten J.M.F.

AU - Ruzzante, Livio

AU - Feron, Romain

AU - Waterhouse, Robert M.

AU - Wu, Yang

AU - Mao, Chunhong

AU - Tu, Zhijian

AU - Sharakhov, Igor V.

AU - Fishman, Veniamin

N1 - Funding Information: The following reagents were obtained through BEI Resources, NIAID, NIH: An. coluzzii , Strain MOPTI, Eggs, MRA-763, contributed by Gregory C. Lanzaro; An. merus , Strain MAF, MRA-1156, contributed by Maureen Coetzee; An. atroparvus , Strain EBRO, Eggs, MRA-493, contributed by Carlos Aranda and Mark Q. Benedict; An. albimanus , Strain STECLA, Eggs, MRA-126, contributed by Mark Q. Benedict. All computations were performed using nodes of the high-throughput cluster of the Novosibirsk State University, and bioinformatics resource center of the Institute of Cytology and Genetics. We are sincerely grateful to Nariman Battulin for fruitful discussions. This work was supported by the NSF grant MCB-1715207, NIH NIAID grants R21AI135298 and R21AI159382, and the USDA National Institute of Food and Agriculture Hatch project 223822 to IVS. The reported study of An. atroparvus was partly funded by RFBR according to the research project no 19-34-50051 to IVS and VL. PacBio sequencing of An. merus was funded by a grant from the University of Lausanne Department of Ecology and Evolution to RMW and NIH grants AI133571 and AI121284 to Z.T. M.J.M.F.R., L.R., R.F., and R.M.W. were supported by Novartis Foundation for medical-biological research grant #18B116 and Swiss National Science Foundation grants PP00P3_170664 and PP00P3_202669. V.L. was partly supported by the Fulbright Foreign Student Program, Grantee ID: 15161026. Hi-C data analysis was supported by the Ministry of Education and Science of Russian Federation, grant #2019-0546 (FSUS-2020-0040). ChIP-seq data analysis was supported by project 121031800061-7 (Mechanisms of genetic control of development, physiological processes and behavior in animals). Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - 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.

AB - 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.

KW - Animals

KW - Anopheles/genetics

KW - Chromatin/genetics

UR - http://www.scopus.com/inward/record.url?scp=85128116780&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/1af26e3d-9a3a-3397-812b-32ba85525647/

U2 - 10.1038/s41467-022-29599-5

DO - 10.1038/s41467-022-29599-5

M3 - Article

C2 - 35413948

AN - SCOPUS:85128116780

VL - 13

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 1960

ER -