Skip to main content
SpringerLink
Log in

Prediction of a conserved pheromone receptor lineage from antennal transcriptomes of the pine sawyer genus Monochamus (Coleoptera: Cerambycidae)

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Longhorned beetles (Cerambycidae) are a diverse family of wood-boring insects, many species of which produce volatile pheromones to attract mates over long distances. The composition and structure of the pheromones remain constant across many cerambycid species, and comparative studies of those groups could, therefore, reveal the chemoreceptors responsible for pheromone detection. Here, we use comparative transcriptomics to identify a candidate pheromone receptor in the large and economically important cerambycid genus Monochamus, males of which produce the aggregation-sex pheromone 2-(undecyloxy)-ethanol (“monochamol”). Antennal transcriptomes of the North American species M. maculosus, M. notatus, and M. scutellatus revealed 60–70 odorant receptors (ORs) in each species, including four lineages of simple orthologs that were highly conserved, highly expressed in both sexes, and upregulated in the flagellomeres where olfactory sensilla are localized. Two of these orthologous lineages, OR29 and OR59, remained highly expressed and conserved when we included a re-annotation of an antennal transcriptome of the Eurasian congener M. alternatus. OR29 is also orthologous to a characterized pheromone receptor in the cerambycid Megacyllene caryae, suggesting it as the most likely candidate for a monochamol receptor and highlighting its potential as a conserved lineage of pheromone receptors within one of the largest families of beetles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability statement

The data that support the findings of this study are openly available in the NCBI Sequence Read Archive (SRA) at https://www.ncbi.nlm.nih.gov/sra, BioProject ID PRJNA821225 and in the supplementary material of this article.

References

  • Allison JD, Borden JH, McIntosh RL, De Groot P, Gries R (2001) Kairomonal response by four Monochamus species. (Coleoptera: Cerambycidae) to bark beetle pheromones. J Chem Ecol 27:633–646

    Article  CAS  Google Scholar 

  • Allison JD, Borden JH, Seybold SJ (2004) A review of the chemical ecology of the Cerambycidae (Coleoptera). Chemoecology 14:123–150

    Article  CAS  Google Scholar 

  • Allison JD, McKenney JL, Millar JG, McElfresh JS, Mitchell RF, Hanks LM (2012) Response of the woodborers Monochamus carolinensis and Monochamus titillator (Coleoptera: Cerambycidae) to known cerambycid pheromones in the presence and absence of the host plant volatile α-pinene. Environ Entomol 41:1587–1596

    Article  CAS  Google Scholar 

  • Anderson AR, Newcomb RD (2021) Olfactory genomics and biotechnology in insect control. In: Blomquist G, Vogt R (eds) Insect pheromone biochemistry and molecular biology, 2nd edn. Academic Press, Cambridge, MA, USA, pp 645–674

    Chapter  Google Scholar 

  • Antony B, Johny J, Montagné N, Jacquin-Joly E, Capoduro R, Cali K, Persaud K, Al-Saleh MA, Pain A (2021) Pheromone receptor of the globally invasive quarantine pest of the palm tree, the red palm weevil (Rhynchophorus ferrugineus). Mol Ecol 30:2025–2039

    Article  CAS  Google Scholar 

  • Bengtsson JM, Gonzalez F, Cattaneo AM, Montagné N, Walker WB, Bengtsson M, Anfora G, Ignell R, Jacquin-Joly E, Witzgall P (2014) A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester. Front Ecol Evol 2:33

    Article  Google Scholar 

  • Bohbot JD, Vernick S (2020) The emergence of insect odorant receptor-based biosensors. Biosensors 10:26

    Article  CAS  Google Scholar 

  • Cerezke HF, Volney WJA (1995) Forest insect pests in the Northwest region. In: Armstrong JA, Ives WGH (eds) Forest insect pests in Canada. Natural Resources Canada, Ottawa, ON, Canada, pp 59–72

    Google Scholar 

  • Dippel S, Kollmann M, Oberhofer G, Montino A, Knoll C, Krala M, Rexer K-H, Frank S, Kumpf R, Schachtner J, Wimmer EA (2016) Morphological and transcriptomic analysis of a beetle chemosensory system reveals a gnathal olfactory center. BMC Biol 14(1):90. https://doi.org/10.1186/s12915-016-0304-z

    Article  CAS  Google Scholar 

  • Dyer LJ, Seabrook WD (1975) Sensilla on the antennal flagellum of the sawyer beetles Monochamus notatus (Drury) and Monochamus scutellatus (Say) (Coleoptera: Cerambycidae). J Morphol 146:513–531

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  Google Scholar 

  • Engsontia P, Sanderson AP, Cobb M, Walden KKO, Robertson HM, Brown S (2008) The red flour beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38(4):387–397. https://doi.org/10.1016/j.ibmb.2007.10.005

    Article  CAS  Google Scholar 

  • Fierke MK, Skabeikis DD, Millar JG, Teale SA, McElfresh JS, Hanks LM (2012) Identification of a male-produced aggregation pheromone for Monochamus scutellatus scutellatus and an attractant for the congener Monochamus notatus (Coleoptera: Cerambycidae). J Econ Entomol 105:2029–2034

    Article  CAS  Google Scholar 

  • Fleischer J, Krieger J (2021) Molecular mechanisms of pheromone detection. In: Blomquist G, Vogt R (eds) Insect pheromone biochemistry and molecular biology, 2nd edn. Academic Press, Cambridge, MA, USA, pp 355–413

    Chapter  Google Scholar 

  • Franco TA, Xu P, Brito NF, Oliveira DS, Wen X, Moreira MF, Unelius CR, Leal WS, Melo AC (2018) Reverse chemical ecology-based approach leading to the accidental discovery of repellents for Rhodnius prolixus, a vector of Chagas diseases refractory to DEET. Insect Biochem Mol Biol 103:46–52

    Article  CAS  Google Scholar 

  • Gorring PS (2019) Gene to genus: systematics and population dynamics in Lamiini Beetles (Coleoptera: Cerambycidae) with focus on Monochamus Dejean. Dissertation, Harvard University

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  • Haack RA, Hérard F, Sun J, Turgeon JJ (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: a worldwide perspective. Annu Rev Entomol 55:521–546

    Article  CAS  Google Scholar 

  • Hansen L, Xu T, Wickham J, Chen Y, Hao D, Hanks LM, Millar JG, Teale SA (2015) Identification of a male-produced pheromone component of the citrus longhorned beetle Anoplophora Chinensis. Plos one 10:e0134358

    Article  Google Scholar 

  • Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711

    Article  CAS  Google Scholar 

  • Hou XQ, Yuvaraj JK, Roberts RE, Zhang DD, Unelius CR, Löfstedt C, Andersson MN (2021) Functional evolution of a bark beetle odorant receptor clade detecting monoterpenoids of different ecological origins. Mol Biol Evol 38:4934–4947

    Article  CAS  Google Scholar 

  • Ji T, Xu Z, Jia Q, Wang G, Hou Y (2021) Non-palm plant volatile α-pinene is detected by antenna-biased expressed odorant receptor 6 in the Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Front Physiol 12:701545

    Article  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  Google Scholar 

  • Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773

    Google Scholar 

  • Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE, Macallister IE, Kavanaugh MP, Wanner KW (2012) Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci USA 109:14081–14086

    Article  CAS  Google Scholar 

  • Lemoine F, Domelevo Entfellner JB, Wilkinson E, Correia D, Dávila Felipe M, De Oliveira T, Gascuel O (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556:452–456

    Article  CAS  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  Google Scholar 

  • McKenna DD, Scully ED, Pauchet Y, Hoover K, Kirsch R, Geib SM, Mitchell RF, Waterhouse RM, Ahn S-J, Arsala D et al (2016) Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface. Genome Biol 17:227

    Article  Google Scholar 

  • Millar JG, Hanks LM (2017) Chemical ecology of cerambycids. In: Wang Q (ed) Cerambycidae of the world: biology and pest management. CRC Press/Taylor & Francis, Boca Raton, FL, USA, pp 161–208

    Google Scholar 

  • Miller DR (2006) Ethanol and (−)-α-pinene: attractant kairomones for some large wood-boring beetles in southeastern USA. J Chem Ecol 32:779–794

    Article  CAS  Google Scholar 

  • Miller DR, Dodds KJ, Eglitis A, Fettig CJ, Hofstetter RW, Langor DW, Mayfield AE III, Munson AS, Poland TM, Raffa KF (2013) Trap lure blend of pine volatiles and bark beetle pheromones for Monochamus species. (Coleoptera: Cerambycidae) in pine forests of Canada and the United States. J Econ Entomol 106:1684–1692

    Article  Google Scholar 

  • Mitchell RF, Andersson MN (2021) Olfactory genomics of the Coleoptera. In: Blomquist G, Vogt R (eds) Insect pheromone biochemistry and molecular biology, 2nd edn. Academic Press, Cambridge, MA, USA, pp 547–590

    Chapter  Google Scholar 

  • Mitchell RF, Hughes DT, Luetje CW, Millar JG, Soriano-Agatón F, Hanks LM, Robertson HM (2012) Sequencing and characterizing odorant receptors of the cerambycid beetle Megacyllene caryae. Insect Biochem Mol Biol 42:499–505

    Article  CAS  Google Scholar 

  • Mitchell RF, Reagel PF, Wong JC, Meier LR, Silva WD, Mongold-Diers J, Millar JG, Hanks LM (2015) Cerambycid beetle species with similar pheromones are segregated by phenology and minor pheromone components. J Chem Ecol 41:431–440

    Article  CAS  Google Scholar 

  • Mitchell RF, Hall LP, Reagel PF, McKenna DD, Baker TC, Hildebrand JG (2017) Odorant receptors and antennal lobe morphology offer a new approach to understanding olfaction in the Asian longhorned beetle. J Comp Physiol A 203:99–109

    Article  CAS  Google Scholar 

  • Mitchell RF, Schneider TM, Schwartz AM, Andersson MN, McKenna DD (2020) The diversity and evolution of odorant receptors in beetles (Coleoptera). Insect Mol Biol 29:77–91

    Article  CAS  Google Scholar 

  • Montagné N, Wanner K, Jacquin-Joly E (2021) Olfactory genomics within the Lepidoptera. In: Blomquist G, Vogt R (eds) Insect pheromone biochemistry and molecular biology, 2nd edn. Academic Press, Cambridge, MA, USA, pp 469–505

    Chapter  Google Scholar 

  • Morimoto K, Iwasaki A (1972) Role of Monochamus alternatus (Coleoptera: Cerambycidae) as a vector of Bursaphelenchus lignicolus (Nematoda: Aphelenchoididae). J Jap for Soc 54:177–183

    Google Scholar 

  • Nehme ME, Trotter RT, Keena MA, McFarland C, Coop J, Hull-Sanders HM, Meng P, De Moraes CM, Mescher MC, Hoover K (2014) Development and evaluation of a trapping system for Anoplophora glabripennis (Coleoptera: Cerambycidae) in the United States. Environ Entomol 43:1034–1044

    Article  CAS  Google Scholar 

  • Oppert B, Muszewska A, Steczkiewicz K, Šatović-Vukšić E, Plohl M, Fabrick JA, Vinokurov KS, Koloniuk I, Johnston JS, Smith TP et al (2022) The genome of Rhyzopertha dominica (Fab.) (Coleoptera: Bostrichidae): adaptation for success. Genes 13:446

    Article  CAS  Google Scholar 

  • Pajares JA, Álvarez G, Ibeas F, Gallego D, Hall DR, Farman DI (2010) Identification and field activity of a male-produced aggregation pheromone in the pine sawyer beetle, Monochamus galloprovincialis. J Chem Ecol 36:570–583

    Article  CAS  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490

    Article  Google Scholar 

  • Qian JL, Mang DZ, Lv GC, Ye J, Li ZQ, Chu B, Sun L, Liu YJ, Zhang LW (2020) Identification and expression profile of olfactory receptor genes based on Apriona germari (Hope) antennal transcriptome. Front Physiol 11:807

    Article  Google Scholar 

  • Ray AM, Barbour JD, McElfresh JS, Moreira JA, Swift I, Wright IM, Žunič A, Mitchell RF, Graham EE, Alten RL, Millar JG (2012) 2, 3-Hexanediols as sex attractants and a female-produced sex pheromone for cerambycid beetles in the prionine genus Tragosoma. J Chem Ecol 38:1151–1158

    Article  CAS  Google Scholar 

  • Ray AM, Millar JG, Moreira JA, McElfresh JS, Mitchell RF, Barbour JD, Hanks LM (2015) North American species of cerambycid beetles in the genus Neoclytus share a common hydroxyhexanone-hexanediol pheromone structural motif. J Econ Entomol 108:1860–1868

    Article  CAS  Google Scholar 

  • Ryall K, Silk P, Webster RP, Gutowski JM, Meng Q, Li Y, Gao W, Fidgen J, Kimoto T, Scarr T, Mastro V (2015) Further evidence that monochamol is attractive to Monochamus (Coleoptera: Cerambycidae) species, with attraction synergised by host plant volatiles and bark beetle (Coleoptera: Curculionidae) pheromones. Can Entomol 147:564–579

    Article  Google Scholar 

  • Solomon JD (1995) Guide to insect borers in North American broadleaf trees and shrubs (No. 706). USDA Forest Service, Washington, DC, USA

    Google Scholar 

  • Teale SA, Wickham JD, Zhang F, Su J, Chen Y, Xiao W, Hanks LM, Millar JG (2011) A male-produced aggregation pheromone of Monochamus alternatus (Coleoptera: Cerambycidae), a major vector of pine wood nematode. J Econ Entomol 104:1592–1598

    Article  CAS  Google Scholar 

  • Wang J, Li DZ, Min SF, Mi F, Zhou SS, Wang MQ (2014) Analysis of chemosensory gene families in the beetle Monochamus alternatus and its parasitoid Dastarcus helophoroides. Comp Biochem Physiol D 11:1–8

    Google Scholar 

  • Wang X, Wang S, Yi J, Li Y, Liu J, Wang J, Xi J (2020) Three host plant volatiles, hexanal, lauric acid, and tetradecane, are detected by an antenna-biased expressed odorant receptor 27 in the dark black chafer Holotrichia parallela. J Agric Food Chem 68(28):7316–7323. https://doi.org/10.1021/acs.jafc.0c00333

    Article  CAS  Google Scholar 

  • Wickham JD, Harrison RD, Lu W, Chen Y, Hanks LM, Millar JG (2021) Rapid assessment of cerambycid beetle biodiversity in a tropical rainforest in Yunnan Province, China, using a multicomponent pheromone lure. Insects 12:277

    Article  Google Scholar 

  • Wu Z, Ye J, Qian J, Purba ER, Zhang Q, Zhang L, Mang D (2022) Identification and expression profile of chemosensory receptor genes in Aromia bungii (Faldermann) antennal transcriptome. Insects 13:96

    Article  Google Scholar 

  • Xu B, Yang Z (2013) PAMLX: a graphical user interface for PAML. Mol Biol Evol 30:2723–2724

    Article  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  Google Scholar 

  • Yuvaraj JK, Roberts RE, Sonntag Y, Hou XQ, Grosse-Wilde E, Machara A, Zhang DD, Hansson BS, Johanson U, Löfstedt C, Andersson MN (2021) Putative ligand binding sites of two functionally characterized bark beetle odorant receptors. BMC Biol 19:1–21

    Article  Google Scholar 

  • Zhang A, Oliver JE, Aldrich JR, Wang B, Mastro VC (2002) Stimulatory beetle volatiles for the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky). Z Naturforsch C 57:553–558

    Article  CAS  Google Scholar 

  • Zhang R, Wang B, Grossi G, Falabella P, Liu Y, Yan S, Lu J, Xi J, Wang G (2017) Molecular basis of alarm pheromone detection in aphids. Curr Biol 27:55–61

    Article  CAS  Google Scholar 

  • Zhao S, Ye Z, Stanton R (2020a) Misuse of RPKM or TPM normalization when comparing across samples and sequencing protocols. RNA 26:903–909

    Article  CAS  Google Scholar 

  • Zhao YJ, Li GC, Zhu JY, Liu NY (2020b) Genome-based analysis reveals a novel SNMP group of the Coleoptera and chemosensory receptors in Rhaphuma horsfieldi. Genomics 112:2713–2728

    Article  CAS  Google Scholar 

  • Zhao Y, Li MC, Konaté MM, Chen L, Das B, Karlovich C, Williams PM, Evrard YA, Doroshow JH, McShane LM (2021) TPM, FPKM, or normalized counts? A comparative study of quantification measures for the analysis of RNA-seq data from the NCI patient-derived models repository. J Transl Med 19:1–15

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Patrick Gorring for comments on an early draft of this manuscript and Nick Boyonoski for assistance collecting insects.

Funding

This work was supported by the University of Wisconsin Oshkosh (to RFM), a Genomics Research and Development Initiative (GRDI) grant (to DD), and by the Canadian Forest Service (to DD and JDA).

Author information

Authors and Affiliations

  1. Department of Biology, University of Wisconsin Oshkosh, 800 Algoma Blvd., Oshkosh, WI, 54901, USA

    Robert F. Mitchell

  2. Canadian Forest Service, Natural Resources Canada, Great Lakes Forestry Centre, Sault Ste. Marie, ON, P6A2E5, Canada

    Daniel Doucet, Susan Bowman, Marc C. Bouwer & Jeremy D. Allison

  3. Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South Africa

    Marc C. Bouwer & Jeremy D. Allison

Authors
  1. Robert F. Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Doucet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan Bowman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marc C. Bouwer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jeremy D. Allison
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RFM, DD, and JDA: designed the study; MCB and JDA: oversaw field collection of samples; DD and SB: performed molecular work and sequencing; RFM: analyzed data and wrote the manuscript; all authors reviewed, edited, and approved the final manuscript.

Corresponding author

Correspondence to Robert F. Mitchell.

Ethics declarations

Conflict of interest

The authors have no competing interests to declare.

Additional information

Handling editor: Kentaro Arikawa.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mitchell, R.F., Doucet, D., Bowman, S. et al. Prediction of a conserved pheromone receptor lineage from antennal transcriptomes of the pine sawyer genus Monochamus (Coleoptera: Cerambycidae). J Comp Physiol A 208, 615–625 (2022). https://doi.org/10.1007/s00359-022-01583-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-022-01583-w

Keywords

Search

Navigation