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

Subjects

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.

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.

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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.

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

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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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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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