TY - JOUR
T1 - Evolutionary origin of OwlRep, a megasatellite DNA associated with adaptation of owl monkeys to nocturnal lifestyle
AU - Nishihara, Hidenori
AU - Stanyon, Roscoe
AU - Kusumi, Junko
AU - Hirai, Hirohisa
AU - Koga, Akihiko
N1 - Funding Information:
We thank Human Genome Sequencing Center, Baylor College of Medicine (https://www.hgsc.bcm.edu/non-human-primates/owl-monkey-genome-project; last accessed January 3, 2018) for the public release of the Aotus nancy-maae (Ma’s night monkey) genome. Computational analyses were partially performed on the supercomputer system of the Institute of Statistical Mathematics. This work was supported by Grants-in-Aid from the MEXT of Japan (grant numbers 15H04427 and 23114005 to A.K.; 26840117 and 17K19424 to H.N.) and a grant from the Italian Ministry of Universities and Research (2015RA7XZS_003 to R.S.).
Funding Information:
We thank Human Genome Sequencing Center, Baylor College of Medicine (https://www.hgsc.bcm.edu/non-human-primates/owl-monkey-genome-project; last accessed January 3, 2018) for the public release of the Aotus nancymaae (Ma’s night monkey) genome. Computational analyses were partially performed on the supercomputer system of the Institute of Statistical Mathematics. This work was supported by Grants-in-Aid from the MEXT of Japan (grant numbers 15H04427 and 23114005 to A.K.; 26840117 and 17K19424 to H.N.) and a grant from the Italian Ministry of Universities and Research (2015RA7XZS_003 to R.S.).
Publisher Copyright:
© The Author 2017.
PY - 2018/1
Y1 - 2018/1
N2 - Rod cells of many nocturnal mammals have a “non-standard” nuclear architecture, which is called the inverted nuclear architecture. Heterochromatin localizes to the central region of the nucleus. This leads to an efficient light transmission to the outer segments of photoreceptors. Rod cells of diurnal mammals have the conventional nuclear architecture. Owl monkeys (genus Aotus) are the only taxon of simian primates that has a nocturnal or cathemeral lifestyle, and this adaptation is widely thought to be secondary. Their rod cells were shown to exhibit an intermediate chromatin distribution: a spherical heterochromatin block was found in the central region of the nucleus although it was less complete than that of typical nocturnal mammals. We recently demonstrated that the primary DNA component of this heterochromatin block was OwlRep, a megasatellite DNA consisting of 187-bp-long repeat units. However, the origin of OwlRep was not known. Here we show that OwlRep was derived from HSAT6, a simple repeat sequence found in the centromere regions of human chromosomes. HSAT6 occurs widely in primates, suggesting that it was already present in the last common ancestor of extant primates. Notably, Strepsirrhini and Tarsiformes apparently carry a single HSAT6 copy, whereas many species of Simiiformes contain multiple copies. Comparison of nucleotide sequences of these copies revealed the entire process of the OwlRep formation. HSAT6, with or without flanking sequences, was segmentally duplicated in New World monkeys. Then, in the owl monkey linage after its divergence from other New World monkeys, a copy of HSAT6 was tandemly amplified, eventually forming a megasatellite DNA.
AB - Rod cells of many nocturnal mammals have a “non-standard” nuclear architecture, which is called the inverted nuclear architecture. Heterochromatin localizes to the central region of the nucleus. This leads to an efficient light transmission to the outer segments of photoreceptors. Rod cells of diurnal mammals have the conventional nuclear architecture. Owl monkeys (genus Aotus) are the only taxon of simian primates that has a nocturnal or cathemeral lifestyle, and this adaptation is widely thought to be secondary. Their rod cells were shown to exhibit an intermediate chromatin distribution: a spherical heterochromatin block was found in the central region of the nucleus although it was less complete than that of typical nocturnal mammals. We recently demonstrated that the primary DNA component of this heterochromatin block was OwlRep, a megasatellite DNA consisting of 187-bp-long repeat units. However, the origin of OwlRep was not known. Here we show that OwlRep was derived from HSAT6, a simple repeat sequence found in the centromere regions of human chromosomes. HSAT6 occurs widely in primates, suggesting that it was already present in the last common ancestor of extant primates. Notably, Strepsirrhini and Tarsiformes apparently carry a single HSAT6 copy, whereas many species of Simiiformes contain multiple copies. Comparison of nucleotide sequences of these copies revealed the entire process of the OwlRep formation. HSAT6, with or without flanking sequences, was segmentally duplicated in New World monkeys. Then, in the owl monkey linage after its divergence from other New World monkeys, a copy of HSAT6 was tandemly amplified, eventually forming a megasatellite DNA.
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U2 - 10.1093/gbe/evx281
DO - 10.1093/gbe/evx281
M3 - Article
C2 - 29294004
AN - SCOPUS:85045949042
VL - 10
SP - 157
EP - 165
JO - Genome Biology and Evolution
JF - Genome Biology and Evolution
SN - 1759-6653
IS - 1
ER -