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Evolutionary shifts in pheromone receptors contribute to speciation in four Helicoverpa species

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Abstract

Male moths utilize their pheromone communication systems to distinguish potential mates from other sympatric species, which contributes to maintaining reproductive isolation and even drives speciation. The molecular mechanisms underlying the evolution of pheromone communication systems are usually studied between closely-related moth species for their similar but divergent traits associated with pheromone production, detection, and/or processing. In this study, we first identified the functional differentiation in two orthologous pheromone receptors, OR14b, and OR16, in four Helicoverpa species, Helicoverpa armigera, H. assulta, H. zea, and H. gelotopoeon. To understand the substrate response specificity of these two PRs, we performed all-atom molecular dynamics simulations of OR14b and OR16 based on AlphaFold2 structural prediction, and molecular docking, allowing us to predict a few key amino acids involved in substrate binding. These candidate residues were further tested and validated by site-directed mutagenesis and functional analysis. These results together identified two hydrophobic amino acids at positions 164 and 232 are the determinants of the response specificity of HarmOR14b and HzeaOR14b to Z9-14:Ald and Z9-16:Ald by directly interacting with the substrates. Interestingly, in OR16 orthologs, we found that position 66 alone determines the specific binding of Z11-16:OH, likely via allosteric interactions. Overall, we have developed an effective integrated method to identify the critical residues for substrate selectivity of ORs and elucidated the molecular mechanism of the diversification of pheromone recognition systems.

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All data generated or analyzed during this study are included in this article (and its Supplementary files).

Abbreviations

OR:

Odorant receptor

Orco:

Odorant receptor co-receptor

PBP:

Pheromone binding protein

SNMP:

Sensory neuron membrane protein

PDE:

Pheromone degrading enzyme

PR:

Pheromone receptor

cRNA:

Caped RNA

TMD:

Transmembrane domain

ECL:

Extracellular loop

cryoEM:

Cryogenic electron microscopy

CGenFF:

CHARMM general force field

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Acknowledgements

We thank Dr. Fred Gould (North Carolina State University, Raleigh, NC, USA) for providing the experimental materials and comments. We also thank Dr. Emmanuelle Jacquin-Joly (INRAE, Sorbonne Universite, CNRS, IRD, UPEC, Universite de Paris, Institute of Ecology and Environmental Sciences of Paris) for helpful discussions. Y.W acknowledges the access to computational resources from the Information Technology Center and State Key Lab of CAD&CG, Zhejiang University.

Funding

This work was funded by National Natural Science Foundation of China (32130089 to G.W., 32272540, 32072509 to Y.L., and 11932017 to P.X.), the National Key R&D Program of China (No. 2021YFF1200404 to Y.W.), the Fundamental Research Funds for the Central Universities of China (No. K20220228 to Y.W.), China Postdoctoral Science Foundation (2020M680785 to S.C.), and the Shenzhen Science and Technology Program (Grant No. KQTD20180411143628272 to G.W.), Central Public-interest Scientific Institution Basal Research Fund (CAAS-ZDRW202108), Projects subsidized by Special Funds for Science Technology Innovation and Industrial Development of Shenzhen Dapeng New District (PT202101-02), and the Agricultural Science and Technology Innovation Program (ASTIP). The funder had no role in study design, data collection and interpretation or manuscript preparation.

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  1. Song Cao and Chen Shi contributed equally.

Authors and Affiliations

  1. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

    Song Cao, Bing Wang, Yang Liu & Guirong Wang

  2. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China

    Song Cao & Guirong Wang

  3. Department of Engineering Mechanics, Zhejiang University, Hangzhou, 310027, China

    Chen Shi & Peng Xiu

  4. College of Life Sciences, Zhejiang University, Hangzhou, 310058, China

    Yong Wang

  5. The Provincial International Science and Technology Cooperation Base On Engineering Biology, International Campus of Zhejiang University, Haining, 314499, China

    Yong Wang

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  1. Song Cao
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Contributions

Conceptualization, YL, GW and YW; conducted experiments, SC, YL, CS and BW; data analysis and visualization, SC and CS; writing—original draft, SC, YL and CS; writing—review and editing, SC, CS, BW, PX, YW, YL and GW; funding acquisition, SC, PX, YW, YL and GW.

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Cao, S., Shi, C., Wang, B. et al. Evolutionary shifts in pheromone receptors contribute to speciation in four Helicoverpa species. Cell. Mol. Life Sci. 80, 199 (2023). https://doi.org/10.1007/s00018-023-04837-1

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