Genomic data and ecological niche modeling reveal an unusually slow rate of molecular evolution in the Cretaceous Eupteleaceae

Living fossils are evidence of long-term sustained ecological success. However, whether living fossils have little molecular changes remains poorly known, particularly in plants. Here, we have introduced a novel method that integrates phylogenomic, comparative genomic, and ecological niche modeling analyses to investigate the rate of molecular evolution of Eupteleaceae, a Cretaceous relict angiosperm family endemic to East Asia. We assembled a high-quality chromosome-level nuclear genome, and the chloroplast and mitochondrial genomes of a member of Eupteleaceae (Euptelea pleiosperma). Our results show that Eupteleaceae is most basal in Ranunculales, the earliest-diverging order in eudicots, and shares an ancient whole-genome duplication event with the other Ranunculales. We document that Eupteleaceae has the slowest rate of molecular changes in the observed angiosperms. The unusually low rate of molecular evolution of Eupteleaceae across all three independent inherited genomes and genes within each of the three genomes is in association with its conserved genome architecture, ancestral woody habit, and conserved niche requirements. Our findings reveal the evolution and adaptation of living fossil plants through large-scale environmental change and also provide new insights into early eudicot diversification.

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Availability of data

All raw sequencing reads generated in this study have been deposited in the NCBI Sequence Read Archive (https://www.ncbi.nlm.nlh.gov/sra) with Bioproject accession number PRJNA980104. The genome assembly sequences and gene annotations have been deposited in GenBank under the accession JASUTR000000000. The sequence alignments used to generate phylogenetic trees have been deposited in the FigShare database (https://doi.org/10.6084/m9.figshare.23295485).

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Acknowledgement

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31030000), the National Natural Science Foundation of China (32170210, 32170238, 31770231, 31770233), the Science, Technology, and Innovation Commission of Shenzhen Municipality of China (RCYX20200714114538196), K.C. Wong Education Foundation (GJTD-2020-05) and Innovation Program of Chinese Academy of Agricultural Sciences.

Author information

1. Contributed equally to this work

Authors and Affiliations

1. State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China Kun-Li Xiang, Lian Lian, Huan-Wen Peng, Hong-Yan Shan, Gui-Xia Xu & Wei Wang
2. Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China Kun-Li Xiang, Wen-Chuang He, Dan Peng, Xiao-Ni Zhang & Zhi-Qiang Wu
3. China National Botanical Garden, Beijing, 100093, China Kun-Li Xiang, Lian Lian, Huan-Wen Peng, Hong-Yan Shan, Gui-Xia Xu & Wei Wang
4. State Key Laboratory of Grassland Agro-Ecosystems and College of Ecology, Lanzhou University, Lanzhou, 730000, China Sheng-Dan Wu
5. University of Chinese Academy of Sciences, Beijing, 100049, China Huan-Wen Peng & Wei Wang
6. College of Landscape Architecture and Life Science/Institute of Special Plants, Chongqing University of Arts and Sciences, Chongqing, 402160, China Hong-Lei Li
7. College of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, 210095, China Jia-Yu Xue
8. Fairylake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen, 518004, China Yang Liu

1. Kun-Li Xiang