Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

Xiaodong Fang; Eviatar Nevo; Lijuan Han; Erez Y. Levanon; Jing Zhao; Aaron Avivi; Denis Larkin; Xuanting Jiang; Sergey Feranchuk; Yabing Zhu; Alla Fishman; Yue Feng; Noa Sher; Zhiqiang Xiong; Thomas Hankeln; Zhiyong Huang; Vera Gorbunova; Lu Zhang; Wei Zhao; Derek E. Wildman; Yingqi Xiong; Andrei Gudkov; Qiumei Zheng; Gideon Rechavi; Sanyang Liu; Lily Bazak; Jie Chen; Binyamin A. Knisbacher; Yao Lu; Imad Shams; Krzysztof Piotr Gajda; Marta Farré-Belmonte; Jaebum Kim; Harris A. Lewin; Jian Ma; Mark Band; Anne Bicker; Angela Kranz; Tobias Mattheus; Hanno Schmidt; Andrei Seluanov; Jorge Azpurua; Michael R. Mcgowen; Eshel Ben Jacob; Kexin Li; Shaoliang Peng; Xiaoqian Zhu; Xiangke Liao; Shuaicheng Li; Anders Krogh; Xin Zhou; Leonid Brodsky; Jun Wang

doi:10.1038/ncomms4966

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

Xiaodong Fang, Eviatar Nevo, Lijuan Han, Erez Y. Levanon, Jing Zhao, Aaron Avivi, Denis Larkin, Xuanting Jiang, Sergey Feranchuk, Yabing Zhu, Alla Fishman, Yue Feng, Noa Sher, Zhiqiang Xiong, Thomas Hankeln, Zhiyong Huang, Vera Gorbunova, Lu Zhang, Wei Zhao, Derek E. WildmanYingqi Xiong, Andrei Gudkov, Qiumei Zheng, Gideon Rechavi, Sanyang Liu, Lily Bazak, Jie Chen, Binyamin A. Knisbacher, Yao Lu, Imad Shams, Krzysztof Piotr Gajda, Marta Farré-Belmonte, Jaebum Kim, Harris A. Lewin, Jian Ma, Mark Band, Anne Bicker, Angela Kranz, Tobias Mattheus, Hanno Schmidt, Andrei Seluanov, Jorge Azpurua, Michael R. Mcgowen, Eshel Ben Jacob, Kexin Li, Shaoliang Peng, Xiaoqian Zhu, Xiangke Liao, Shuaicheng Li, Anders Krogh, Xin Zhou, Leonid Brodsky, Jun Wang

Department of Life Sciences

Research output: Contribution to journal › Article › peer-review

125 Citations (Scopus)

Abstract

The blind mole rat (BMR), Spalax galili, is an excellent model for studying mammalian adaptation to life underground and medical applications. The BMR spends its entire life underground, protecting itself from predators and climatic fluctuations while challenging it with multiple stressors such as darkness, hypoxia, hypercapnia, energetics and high pathonecity. Here we sequence and analyse the BMR genome and transcriptome, highlighting the possible genomic adaptive responses to the underground stressors. Our results show high rates of RNA/DNA editing, reduced chromosome rearrangements, an over-representation of short interspersed elements (SINEs) probably linked to hypoxia tolerance, degeneration of vision and progression of photoperiodic perception, tolerance to hypercapnia and hypoxia and resistance to cancer. The remarkable traits of the BMR, together with its genomic and transcriptomic information, enhance our understanding of adaptation to extreme environments and will enable the utilization of BMR models for biomedical research in the fight against cancer, stroke and cardiovascular diseases.

Original language	English
Article number	3966
Journal	Nature Communications
Volume	5
DOIs	https://doi.org/10.1038/ncomms4966
Publication status	Published - 03 Jun 2014

Keywords

Adaptation, Physiological/genetics
Animals
Darkness
Evolution, Molecular
Gene Expression Profiling
Genome
Hypercapnia
Hypoxia
RNA Editing/genetics
Short Interspersed Nucleotide Elements
Spalax/genetics
Stress, Physiological
Transcriptome/genetics

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10.1038/ncomms4966

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Fang, X., Nevo, E., Han, L., Levanon, E. Y., Zhao, J., Avivi, A., Larkin, D., Jiang, X., Feranchuk, S., Zhu, Y., Fishman, A., Feng, Y., Sher, N., Xiong, Z., Hankeln, T., Huang, Z., Gorbunova, V., Zhang, L., Zhao, W., ... Wang, J. (2014). Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax. Nature Communications, 5, Article 3966. https://doi.org/10.1038/ncomms4966

@article{f44ea6b4a7134e239443474b1a4ba291,

title = "Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax",

abstract = "The blind mole rat (BMR), Spalax galili, is an excellent model for studying mammalian adaptation to life underground and medical applications. The BMR spends its entire life underground, protecting itself from predators and climatic fluctuations while challenging it with multiple stressors such as darkness, hypoxia, hypercapnia, energetics and high pathonecity. Here we sequence and analyse the BMR genome and transcriptome, highlighting the possible genomic adaptive responses to the underground stressors. Our results show high rates of RNA/DNA editing, reduced chromosome rearrangements, an over-representation of short interspersed elements (SINEs) probably linked to hypoxia tolerance, degeneration of vision and progression of photoperiodic perception, tolerance to hypercapnia and hypoxia and resistance to cancer. The remarkable traits of the BMR, together with its genomic and transcriptomic information, enhance our understanding of adaptation to extreme environments and will enable the utilization of BMR models for biomedical research in the fight against cancer, stroke and cardiovascular diseases.",

keywords = "Adaptation, Physiological/genetics, Animals, Darkness, Evolution, Molecular, Gene Expression Profiling, Genome, Hypercapnia, Hypoxia, RNA Editing/genetics, Short Interspersed Nucleotide Elements, Spalax/genetics, Stress, Physiological, Transcriptome/genetics",

author = "Xiaodong Fang and Eviatar Nevo and Lijuan Han and Levanon, {Erez Y.} and Jing Zhao and Aaron Avivi and Denis Larkin and Xuanting Jiang and Sergey Feranchuk and Yabing Zhu and Alla Fishman and Yue Feng and Noa Sher and Zhiqiang Xiong and Thomas Hankeln and Zhiyong Huang and Vera Gorbunova and Lu Zhang and Wei Zhao and Wildman, {Derek E.} and Yingqi Xiong and Andrei Gudkov and Qiumei Zheng and Gideon Rechavi and Sanyang Liu and Lily Bazak and Jie Chen and Knisbacher, {Binyamin A.} and Yao Lu and Imad Shams and Gajda, {Krzysztof Piotr} and Marta Farr{\'e}-Belmonte and Jaebum Kim and Lewin, {Harris A.} and Jian Ma and Mark Band and Anne Bicker and Angela Kranz and Tobias Mattheus and Hanno Schmidt and Andrei Seluanov and Jorge Azpurua and Mcgowen, {Michael R.} and {Ben Jacob}, Eshel and Kexin Li and Shaoliang Peng and Xiaoqian Zhu and Xiangke Liao and Shuaicheng Li and Anders Krogh and Xin Zhou and Leonid Brodsky and Jun Wang",

note = "Funding Information: This project was primarily financed by the Laszlo N. Tauber Family Foundation and secondarily by the National Natural Science Foundation of China (31171190). E.N. thanks the Ancell Teicher Research Foundation for Genetics and Molecular Evolution for financial support. L. Brodsky and S.F. were partly sponsored by the Defense Advanced Research Projects Agency (DARPA) Grant HR0011-11-C-0094. D.L., K.G., M.F., J.K., H.A.L. and J.M. were supported in part by BBSRC grant BB/J010170/1 and PL-Grid Infrastructure. T.H. and H.S. acknowledge the support by the University of Mainz Center for Computational Sciences (SRFN) and the Stiftung Innovation Rhineland-Palatinate. A.A. acknowledges partial support by the Israel Cancer Association (ICA). A.A. and M.B. acknowledge partial support by the US-Israel Binational Foundation (BSF). We thank the TianHe research and development team of the National University of Defense Technology (NUDT) for testing, optimizing and deploying the software on TianHe-2 supercomputers.",

year = "2014",

month = jun,

day = "3",

doi = "10.1038/ncomms4966",

language = "English",

volume = "5",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Springer Nature",

}

Fang, X, Nevo, E, Han, L, Levanon, EY, Zhao, J, Avivi, A, Larkin, D, Jiang, X, Feranchuk, S, Zhu, Y, Fishman, A, Feng, Y, Sher, N, Xiong, Z, Hankeln, T, Huang, Z, Gorbunova, V, Zhang, L, Zhao, W, Wildman, DE, Xiong, Y, Gudkov, A, Zheng, Q, Rechavi, G, Liu, S, Bazak, L, Chen, J, Knisbacher, BA, Lu, Y, Shams, I, Gajda, KP, Farré-Belmonte, M, Kim, J, Lewin, HA, Ma, J, Band, M, Bicker, A, Kranz, A, Mattheus, T, Schmidt, H, Seluanov, A, Azpurua, J, Mcgowen, MR, Ben Jacob, E, Li, K, Peng, S, Zhu, X, Liao, X, Li, S, Krogh, A, Zhou, X, Brodsky, L & Wang, J 2014, 'Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax', Nature Communications, vol. 5, 3966. https://doi.org/10.1038/ncomms4966

TY - JOUR

T1 - Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

AU - Fang, Xiaodong

AU - Nevo, Eviatar

AU - Han, Lijuan

AU - Levanon, Erez Y.

AU - Zhao, Jing

AU - Avivi, Aaron

AU - Larkin, Denis

AU - Jiang, Xuanting

AU - Feranchuk, Sergey

AU - Zhu, Yabing

AU - Fishman, Alla

AU - Feng, Yue

AU - Sher, Noa

AU - Xiong, Zhiqiang

AU - Hankeln, Thomas

AU - Huang, Zhiyong

AU - Gorbunova, Vera

AU - Zhang, Lu

AU - Zhao, Wei

AU - Wildman, Derek E.

AU - Xiong, Yingqi

AU - Gudkov, Andrei

AU - Zheng, Qiumei

AU - Rechavi, Gideon

AU - Liu, Sanyang

AU - Bazak, Lily

AU - Chen, Jie

AU - Knisbacher, Binyamin A.

AU - Lu, Yao

AU - Shams, Imad

AU - Gajda, Krzysztof Piotr

AU - Farré-Belmonte, Marta

AU - Kim, Jaebum

AU - Lewin, Harris A.

AU - Ma, Jian

AU - Band, Mark

AU - Bicker, Anne

AU - Kranz, Angela

AU - Mattheus, Tobias

AU - Schmidt, Hanno

AU - Seluanov, Andrei

AU - Azpurua, Jorge

AU - Mcgowen, Michael R.

AU - Ben Jacob, Eshel

AU - Li, Kexin

AU - Peng, Shaoliang

AU - Zhu, Xiaoqian

AU - Liao, Xiangke

AU - Li, Shuaicheng

AU - Krogh, Anders

AU - Zhou, Xin

AU - Brodsky, Leonid

AU - Wang, Jun

N1 - Funding Information: This project was primarily financed by the Laszlo N. Tauber Family Foundation and secondarily by the National Natural Science Foundation of China (31171190). E.N. thanks the Ancell Teicher Research Foundation for Genetics and Molecular Evolution for financial support. L. Brodsky and S.F. were partly sponsored by the Defense Advanced Research Projects Agency (DARPA) Grant HR0011-11-C-0094. D.L., K.G., M.F., J.K., H.A.L. and J.M. were supported in part by BBSRC grant BB/J010170/1 and PL-Grid Infrastructure. T.H. and H.S. acknowledge the support by the University of Mainz Center for Computational Sciences (SRFN) and the Stiftung Innovation Rhineland-Palatinate. A.A. acknowledges partial support by the Israel Cancer Association (ICA). A.A. and M.B. acknowledge partial support by the US-Israel Binational Foundation (BSF). We thank the TianHe research and development team of the National University of Defense Technology (NUDT) for testing, optimizing and deploying the software on TianHe-2 supercomputers.

PY - 2014/6/3

Y1 - 2014/6/3

N2 - The blind mole rat (BMR), Spalax galili, is an excellent model for studying mammalian adaptation to life underground and medical applications. The BMR spends its entire life underground, protecting itself from predators and climatic fluctuations while challenging it with multiple stressors such as darkness, hypoxia, hypercapnia, energetics and high pathonecity. Here we sequence and analyse the BMR genome and transcriptome, highlighting the possible genomic adaptive responses to the underground stressors. Our results show high rates of RNA/DNA editing, reduced chromosome rearrangements, an over-representation of short interspersed elements (SINEs) probably linked to hypoxia tolerance, degeneration of vision and progression of photoperiodic perception, tolerance to hypercapnia and hypoxia and resistance to cancer. The remarkable traits of the BMR, together with its genomic and transcriptomic information, enhance our understanding of adaptation to extreme environments and will enable the utilization of BMR models for biomedical research in the fight against cancer, stroke and cardiovascular diseases.

AB - The blind mole rat (BMR), Spalax galili, is an excellent model for studying mammalian adaptation to life underground and medical applications. The BMR spends its entire life underground, protecting itself from predators and climatic fluctuations while challenging it with multiple stressors such as darkness, hypoxia, hypercapnia, energetics and high pathonecity. Here we sequence and analyse the BMR genome and transcriptome, highlighting the possible genomic adaptive responses to the underground stressors. Our results show high rates of RNA/DNA editing, reduced chromosome rearrangements, an over-representation of short interspersed elements (SINEs) probably linked to hypoxia tolerance, degeneration of vision and progression of photoperiodic perception, tolerance to hypercapnia and hypoxia and resistance to cancer. The remarkable traits of the BMR, together with its genomic and transcriptomic information, enhance our understanding of adaptation to extreme environments and will enable the utilization of BMR models for biomedical research in the fight against cancer, stroke and cardiovascular diseases.

KW - Adaptation, Physiological/genetics

KW - Animals

KW - Darkness

KW - Evolution, Molecular

KW - Gene Expression Profiling

KW - Genome

KW - Hypercapnia

KW - Hypoxia

KW - RNA Editing/genetics

KW - Short Interspersed Nucleotide Elements

KW - Spalax/genetics

KW - Stress, Physiological

KW - Transcriptome/genetics

UR - http://www.scopus.com/inward/record.url?scp=84901937260&partnerID=8YFLogxK

U2 - 10.1038/ncomms4966

DO - 10.1038/ncomms4966

M3 - Article

C2 - 24892994

SN - 2041-1723

VL - 5

JO - Nature Communications

JF - Nature Communications

M1 - 3966

ER -

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

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Keywords

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Using Reference -assisted chromosome assemblies to study chromosome structures and evolution in vertebrates

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