Adaptive evolution of the enigmatic Takakia now facing climate change in Tibet.

DNA repair UV radiation abiotic stress adaptive evolution development fast-evolving genome gene expansion global warming molecular clock paleontology

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
17 08 2023
Historique:
received: 30 06 2022
revised: 23 03 2023
accepted: 03 07 2023
medline: 21 8 2023
pubmed: 11 8 2023
entrez: 10 8 2023
Statut: ppublish

Résumé

The most extreme environments are the most vulnerable to transformation under a rapidly changing climate. These ecosystems harbor some of the most specialized species, which will likely suffer the highest extinction rates. We document the steepest temperature increase (2010-2021) on record at altitudes of above 4,000 m, triggering a decline of the relictual and highly adapted moss Takakia lepidozioides. Its de-novo-sequenced genome with 27,467 protein-coding genes includes distinct adaptations to abiotic stresses and comprises the largest number of fast-evolving genes under positive selection. The uplift of the study site in the last 65 million years has resulted in life-threatening UV-B radiation and drastically reduced temperatures, and we detected several of the molecular adaptations of Takakia to these environmental changes. Surprisingly, specific morphological features likely occurred earlier than 165 mya in much warmer environments. Following nearly 400 million years of evolution and resilience, this species is now facing extinction.

Identifiants

pubmed: 37562403
pii: S0092-8674(23)00736-5
doi: 10.1016/j.cell.2023.07.003
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3558-3576.e17

Informations de copyright

Copyright © 2023 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Ruoyang Hu (R)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China; State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100193, China.

Xuedong Li (X)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Yong Hu (Y)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Runjie Zhang (R)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Qiang Lv (Q)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Min Zhang (M)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Xianyong Sheng (X)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Feng Zhao (F)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Zhijia Chen (Z)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Yuhan Ding (Y)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Huan Yuan (H)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Xiaofeng Wu (X)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Shuang Xing (S)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Xiaoyu Yan (X)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Fang Bao (F)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Ping Wan (P)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Lihong Xiao (L)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China; State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, Zhejiang 311300, China.

Xiaoqin Wang (X)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Wei Xiao (W)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China.

Eva L Decker (EL)

Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany.

Nico van Gessel (N)

Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany.

Hugues Renault (H)

Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany; Institut de Biologie Moléculaire des Plantes (IBMP), CNRS, University of Strasbourg, 67084 Strasbourg, France.

Gertrud Wiedemann (G)

Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany; Inselspital, University of Bern, 3010 Bern, Switzerland.

Nelly A Horst (NA)

Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany; MetaSystems Hard & Software GmbH, 68804 Altlussheim, Germany.

Fabian B Haas (FB)

Department of Biology, University of Marburg, 35043 Marburg, Germany.

Per K I Wilhelmsson (PKI)

Department of Biology, University of Marburg, 35043 Marburg, Germany.

Kristian K Ullrich (KK)

Department of Biology, University of Marburg, 35043 Marburg, Germany; Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, 24306 Plön, Germany.

Eva Neumann (E)

Department of Biology, University of Marburg, 35043 Marburg, Germany.

Bin Lv (B)

Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada; Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan 610041, China.

Chengzhi Liang (C)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.

Huilong Du (H)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; School of Life Sciences, Institute of Life Sciences and Green Development, Hebei University, Baoding, Hebei 071002, China.

Hongwei Lu (H)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, Guangdong 518055, China.

Qiang Gao (Q)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; Genomics and Genetic Engineering Laboratory of Ornamental Plants, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310058, China.

Zhukuan Cheng (Z)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; Key Laboratory of Plant Functional Genomics of the Ministry of Education, Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, Jiangsu 225009, China.

Hanli You (H)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; Key Laboratory of Plant Functional Genomics of the Ministry of Education, Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, Jiangsu 225009, China.

Peiyong Xin (P)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.

Jinfang Chu (J)

National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China.

Chien-Hsun Huang (CH)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai 200433, China; Key Laboratory of Forage and Endemic Crop Biology, Ministry of Education, School of Life Sciences, Inner Mongolia University, Hohhot 010031, China.

Yang Liu (Y)

Department of Ecology and Evolutionary Biology, University of Connecticut, Unit 3043, Storrs, CT 06269, USA; Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen, Guangdong 518004, China; State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen, Guangdong 518085, China.

Shanshan Dong (S)

Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen, Guangdong 518004, China.

Liangsheng Zhang (L)

Genomics and Genetic Engineering Laboratory of Ornamental Plants, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310058, China.

Fei Chen (F)

Sanya Nanfan Research Institute from Hainan University, Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China.

Lei Deng (L)

College of Resource Environment and Tourism, CNU, Beijing 100048, China.

Fuzhou Duan (F)

College of Resource Environment and Tourism, CNU, Beijing 100048, China.

Wenji Zhao (W)

College of Resource Environment and Tourism, CNU, Beijing 100048, China.

Kai Li (K)

Department of Chemistry, CNU, Beijing 100048, China.

Zhongfeng Li (Z)

Department of Chemistry, CNU, Beijing 100048, China.

Xingru Li (X)

Department of Chemistry, CNU, Beijing 100048, China.

Hengjian Cui (H)

School of Mathematical Sciences, CNU, Beijing 100048, China.

Yong E Zhang (YE)

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

Chuan Ma (C)

State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100193, China.

Ruiliang Zhu (R)

Department of Biology, School of Life Sciences, East China Normal University, Shanghai 200241, China.

Yu Jia (Y)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.

Meizhi Wang (M)

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.

Mitsuyasu Hasebe (M)

Division of Evolutionary Biology, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; Department of Basic Biology, The Graduate School for Advanced Studies (SOKENDAI), Okazaki 444-8585, Japan.

Jinzhong Fu (J)

Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.

Bernard Goffinet (B)

Department of Ecology and Evolutionary Biology, University of Connecticut, Unit 3043, Storrs, CT 06269, USA.

Hong Ma (H)

Department of Biology, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802, USA.

Stefan A Rensing (SA)

Department of Biology, University of Marburg, 35043 Marburg, Germany; Faculty of Chemistry and Pharmacy, University of Freiburg, 79104 Freiburg, Germany.

Ralf Reski (R)

Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany; Signalling Research Centres BIOSS and CIBSS, University of Freiburg, 79104 Freiburg, Germany. Electronic address: ralf.reski@biologie.uni-freiburg.de.

Yikun He (Y)

Beijing Key Laboratory of Plant Gene Resources and Biotechnology for Carbon Reduction and Environmental Improvement, College of Life Sciences, Capital Normal University (CNU), Beijing 100048, China. Electronic address: yhe@cnu.edu.cn.

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