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Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association

Nature Ecology & Evolution volume 5, pages 974–986 (2021)Cite this article

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Abstract

Many insects metamorphose from antagonistic larvae into mutualistic adult pollinators, with reciprocal adaptation leading to specialized insect–plant associations. It remains unknown how such interactions are established at molecular level. Here we assemble high-quality genomes of a fig species, Ficus pumila var. pumila, and its specific pollinating wasp, Wiebesia pumilae. We combine multi-omics with validation experiments to reveal molecular mechanisms underlying this specialized interaction. In the plant, we identify the specific compound attracting pollinators and validate the function of several key genes regulating its biosynthesis. In the pollinator, we find a highly reduced number of odorant-binding protein genes and an odorant-binding protein mainly binding the attractant. During antagonistic interaction, we find similar chemical profiles and turnovers throughout the development of galled ovules and seeds, and a significant contraction of detoxification-related gene families in the pollinator. Our study identifies some key genes bridging coevolved mutualists, establishing expectations for more diffuse insect–pollinator systems.

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Fig. 1: Fig–pollinator mutualism between F. pumila var. pumila and Wiebesia pumilae, and determination of the compound attracting W. pumilae.
Fig. 2: Molecular mechanisms of the specific host identification of W. pumilae.
Fig. 3: Regulation of gene expression in attractant biosynthesis in figs of F. pumila var. pumila.
Fig. 4: Metabolic and genomic signature of antagonistic interaction between F. pumila var. pumila and W. pumilae.

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Data availability

The data that support the findings of this study have been deposited in the CNSA (https://db.cngb.org/cnsa/) of CNGBdb with accession code CNP0000674.

Code availability

All analyses in this study were conducted using published programs, and all codes for data analysis are provided in the Methods.

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Acknowledgements

We thank Y.-J. Wang, Q.-C. Zhu, Q. Sun, Q.-Y. Li, J.-W. Wang, T.-L. Xu, Y. Chen, F.-L. Wei, G.-C. Shen, X.-L. Wen and L.-S. Li for their kind help in field experiments; X.-L. Wen, L.-S. Li and the Public Technology Service Center of XTBG (CAS) for assisting active VOCs analysis; and X.-G. Mao, P.-Y. Hua and D.-Y. Zhang for constructive suggestions in data analysis. This work is supported by NSFC grants 31630008 and 31870356 (X.-Y.C.) and 31870359 (G.W.), and a Talents 1000 Fellowship of Shaanxi Province (D.W.D.). S.T.S. acknowledges departmental support from Harper Adams University.

Author information

Author notes

  1. These authors contributed equally: Rong Wang, Yang Yang, Yi Jing, Simon T. Segar.

Authors and Affiliations

  1. Zhejiang Tiantong Forest Ecosystem National Observation and Research Station, Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration, School of Ecological and Environmental Sciences, East China Normal University, Shanghai, China

    Rong Wang, Yang Yang, Yu Zhang, Shan Chen, Yuan-Yuan Ding, Kai Jiang, Yuan-Yuan Li, Xin Tong, Jing-Jun Yang & Xiao-Yong Chen

  2. Shanghai Institute of Pollution Control and Ecological Security, Shanghai, China

    Rong Wang & Xiao-Yong Chen

  3. BGI Genomics, BGI-Shenzhen, Shenzhen, China

    Yi Jing, Qing-Feng Liu, Qiang Gao, Huan-Ming Yang, Ye Yin & Zhen Yue

  4. Agriculture and Environment Department, Harper Adams University, Newport, UK

    Simon T. Segar

  5. CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China

    Gang Wang, Jin Chen & Ping Wen

  6. Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang, China

    Yan Chen

  7. INRAE, UMR 1062 CBGP, Montferrier-sur-Lez, France

    Astrid Cruaud & Jean-Yves Rasplus

  8. College of Life Sciences, Northwest University, Xi’an, China

    Derek W. Dunn

  9. Department of Biological and Marine Science, University of Hull, Hull, UK

    Philip M. Gilmartin

  10. CEFE, CNRS, University of Montpellier, Paul Valéry University Montpellier, EPHE, IRD, Montpellier, France

    Finn Kjellberg

  11. School of Life Sciences, East China Normal University, Shanghai, China

    Hong-Qing Li

  12. Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China

    Jian-Quan Liu

  13. School of Life Sciences, Guangzhou University, Guangzhou, China

    Min Liu

  14. Department of Biology, University of Maryland, College Park, MD, USA

    Carlos A. Machado

  15. Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Ray Ming

  16. Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China

    Xing-Tan Zhang

  17. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, China

    Yuan-Ye Zhang

  18. Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

    Hui Yu

  19. School of Life Sciences, Qufu Normal University, Qufu, China

    Hui Yu

  20. School of Biology, University of Leeds, Leeds, UK

    Stephen G. Compton

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  1. Rong Wang
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  2. Yang Yang
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Contributions

X.-Y.C. and R.W. conceived and designed the study. R.W., Y. Yang, S.G.C., S.T.S., H.Y. and Z.Y. conducted the experiments and analysed data. Y.J., Q.-F.L., H.Y., Y.-Y.Z., G.W., J.C., R.M., S.C., Y.C., D.W.D., H.-Q.L., M.L., Y.-Y.D., Y.-Y.L., X.T., P.W., J.-J.Y., X.-T.Z., Q.G., Y. Yin, K.J. and H.-M.Y. contributed to data acquisition and data analyses. R.W., S.T.S., S.G.C., J.-Q.L., J.-Y.R., F.K., C.A.M, A.C., P.M.G., Y.-Y.Z. and X.-Y.C. edited the manuscript. All authors contributed to writing the manuscript.

Corresponding authors

Correspondence to Hui Yu, Zhen Yue, Stephen G. Compton or Xiao-Yong Chen.

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Competing interests

The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks Shuqing Xu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–18, Tables 1–17 and references.

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Wang, R., Yang, Y., Jing, Y. et al. Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association. Nat Ecol Evol 5, 974–986 (2021). https://doi.org/10.1038/s41559-021-01469-1

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