TY - JOUR
T1 - Comparative genome microsynteny illuminates the fast evolution of nuclear mitochondrial segments (NUMTs) in mammals
AU - Uvizl, Marek
AU - Puechmaille, Sebastien J.
AU - Power, Sarahjane
AU - Pippel, Martin
AU - Carthy, Samuel
AU - Haerty, Wilfried
AU - Myers, Eugene W.
AU - Teeling, Emma C.
AU - Huang, Zixia
N1 - Data Availability Statement: The publicly available genome, mitogenome, and RNA-Seq data used in this study are documented in the supplementary tables S1 and S13, Supplementary Material online. The intermediate data supporting the conclusions can be available at the GitHub page (https://github.com/huangzixia/NUMT_evolution_in_mammals).
Funding Information: This study is supported by the Irish Research Council Laureate Bursary Grant (No. 74725) and the UCD seed funding (No. 68674) to Z.H., the Irish Research Council Laureate Award IRCLA/2017/58 and Science Foundation Ireland Future Frontiers 19/FFP/6790 awarded to E.C.T., and the Junior Chair from the Institut Universitaire de France awarded to S.J.P.
PY - 2024/1
Y1 - 2024/1
N2 - The escape of DNA from mitochondria into the nuclear genome (nuclear mitochondrial DNA, NUMT) is an ongoing process. Although pervasively observed in eukaryotic genomes, their evolutionary trajectories in a mammal-wide context are poorly understood. The main challenge lies in the orthology assignment of NUMTs across species due to their fast evolution and chromosomal rearrangements over the past 200 million years. To address this issue, we systematically investigated the characteristics of NUMT insertions in 45 mammalian genomes and established a novel, synteny-based method to accurately predict orthologous NUMTs and ascertain their evolution across mammals. With a series of comparative analyses across taxa, we revealed that NUMTs may originate from nonrandom regions in mtDNA, are likely found in transposon-rich and intergenic regions, and unlikely code for functional proteins. Using our synteny-based approach, we leveraged 630 pairwise comparisons of genome-wide microsynteny and predicted the NUMT orthology relationships across 36 mammals. With the phylogenetic patterns of NUMT presence-And-Absence across taxa, we constructed the ancestral state of NUMTs given the mammal tree using a coalescent method. We found support on the ancestral node of Fereuungulata within Laurasiatheria, whose subordinal relationships are still controversial. This study broadens our knowledge on NUMT insertion and evolution in mammalian genomes and highlights the merit of NUMTs as alternative genetic markers in phylogenetic inference.
AB - The escape of DNA from mitochondria into the nuclear genome (nuclear mitochondrial DNA, NUMT) is an ongoing process. Although pervasively observed in eukaryotic genomes, their evolutionary trajectories in a mammal-wide context are poorly understood. The main challenge lies in the orthology assignment of NUMTs across species due to their fast evolution and chromosomal rearrangements over the past 200 million years. To address this issue, we systematically investigated the characteristics of NUMT insertions in 45 mammalian genomes and established a novel, synteny-based method to accurately predict orthologous NUMTs and ascertain their evolution across mammals. With a series of comparative analyses across taxa, we revealed that NUMTs may originate from nonrandom regions in mtDNA, are likely found in transposon-rich and intergenic regions, and unlikely code for functional proteins. Using our synteny-based approach, we leveraged 630 pairwise comparisons of genome-wide microsynteny and predicted the NUMT orthology relationships across 36 mammals. With the phylogenetic patterns of NUMT presence-And-Absence across taxa, we constructed the ancestral state of NUMTs given the mammal tree using a coalescent method. We found support on the ancestral node of Fereuungulata within Laurasiatheria, whose subordinal relationships are still controversial. This study broadens our knowledge on NUMT insertion and evolution in mammalian genomes and highlights the merit of NUMTs as alternative genetic markers in phylogenetic inference.
KW - evolution
KW - genome microsynteny
KW - mammal
KW - nuclear mitochondrial DNA segment (NUMT)
UR - http://www.scopus.com/inward/record.url?scp=85182091198&partnerID=8YFLogxK
U2 - 10.1093/molbev/msad278
DO - 10.1093/molbev/msad278
M3 - Article
C2 - 38124445
AN - SCOPUS:85182091198
VL - 41
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
SN - 0737-4038
IS - 1
M1 - msad278
ER -