Advertisement

SNMP1 and odorant receptors are co-expressed in olfactory neurons of the labial and maxillary palps from the desert locust Schistocerca gregaria (Orthoptera: Acrididae)

  • 210 Accesses

  • 1 Citations

Abstract

In insects, pheromones are detected by olfactory sensory neurons (OSNs) of the antennae that co-express pheromone receptors (PRs) and the “sensory neuron membrane protein 1” (SNMP1). Beyond its relevance for pheromone detection via the antenna, little is known about a potential expression and functional role of SNMP1 in cells of other chemosensory appendages. Here, we report that in the desert locust Schistocerca gregaria, SNMP1 is also expressed in the labial and maxillary palps of the mouthparts. In the palps, the SNMP1-positive cells were situated next to the so-called terminal sensilla that are considered as chemosensory. Moreover, the SNMP1-positive cells of the palps expressed the “odorant receptor co-receptor” (Orco), a marker for OSNs endowed with odorant receptors (ORs), suggesting that these cells are olfactory. With respect to an olfactory function of the SNMP1-positive cells, further analyses examining a possible expression of ORs (notably putative PRs) in the labial and maxillary palps revealed that several members of a particular OR subfamily from S. gregaria, the b-OR group, are co-expressed with SNMP1 in cells of the palps. Interestingly, b-OR types co-expressed with SNMP1 in antennal OSNs were also co-expressed with SNMP1 in cells of the palps, indicating a specific pairing in the expression of SNMP1 and given ORs in both antennae and palps. The co-expression of SNMP1 and certain b-ORs that are regarded as candidate PRs opens up the possibility that chemosensory cells on the palps of the desert locust may contribute to pheromone detection.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Abbreviations

b-OR(s):

Member(s) of the basal odorant receptor subfamily of odorant receptors from Schistocerca gregaria

DAPI:

4′,6-Diamidino-2-phenylindole

dNTP:

2′-Deoxynucleoside 5′-triphosphate

FISH:

Fluorescence in situ hybridization

OR(s):

Odorant receptor(s)

Orco:

Odorant receptor co-receptor

OSN(s):

Olfactory sensory neuron(s)

PCR:

Polymerase chain reaction

PR(s):

Pheromone receptor(s)

-RT:

Without reverse transcriptase

SgreOR:

Odorant receptor from Schistocerca gregaria

SNMP1:

Sensory neuron membrane protein 1

References

  1. Applebaum SW, Heifetz Y (1999) Density-dependent physiological phase in insects. Annu Rev Entomol 44:317–341

  2. Benton R, Vannice KS, Vosshall LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–293

  3. Blaney WM (1974) Electrophysiological responses of terminal sensilla on maxillary palps of Locusta migratoria (L) to some electrolytes and nonelectrolytes. J Exp Biol 60:275–293

  4. Blaney WM (1977) The ultrastructure of an olfactory sensillum on the maxillary palps of Locusta migratoria (L.). Cell Tissue Res 184:397–409

  5. Blaney WM, Chapman RF (1969a) The anatomy and histology of the maxillary palp of Schistocerca gregaria (Orthoptera Acrididae). J Zool 157:509–535

  6. Blaney WM, Chapman RF (1969b) The fine structure of the terminal sensilla on the maxillary palps of Schistocerca gregaria (Forskal) (Orthoptera, Acrididae). Z Zellforsch Mikrosk Anat 99:74–97

  7. Blaney WM, Chapman RF, Cook AG (1971) The structure of the terminal sensilla on the maxillary palps of Locusta migratoria (L.), and changes associated with moulting. Z Zellforsch Mikrosk Anat 121:48–68

  8. Blaney WM, Duckett AM (1975) Significance of palpation by maxillary palps of Locusta migratoria (L) - electrophysiological and behavioral study. J Exp Biol 63:701–712

  9. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547

  10. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–841

  11. Dweck HK, Ebrahim SA, Kromann S, Bown D, Hillbur Y, Sachse S, Hansson BS, Stensmyr MC (2013) Olfactory preference for egg laying on citrus substrates in Drosophila. Curr Biol 23:2472–2480

  12. Ferenz HJ, Seidelmann K (2003) Pheromones in relation to aggregation and reproduction in desert locusts. Physiol Entomol 28:11–18

  13. Ferveur JF (1997) The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. Bioessays 19:353–358

  14. Fleischer J, Krieger J (2018) Insect pheromone receptors - key elements in sensing intraspecific chemical signals. Front Cell Neurosci 12:425

  15. Forstner M, Gohl T, Gondesen I, Raming K, Breer H, Krieger J (2008) Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem Senses 33:291–299

  16. German PF, van der Poel S, Carraher C, Kralicek AV, Newcomb RD (2013) Insights into subunit interactions within the insect olfactory receptor complex using FRET. Insect Biochem Mol Biol 43:138–145

  17. Gomez-Diaz C, Bargeton B, Abuin L, Bukar N, Reina JH, Bartoi T, Graf M, Ong H, Ulbrich MH, Masson JF, Benton R (2016) A CD36 ectodomain mediates insect pheromone detection via a putative tunnelling mechanism. Nat Commun 7:11866

  18. Gomez-Diaz C, Benton R (2013) The joy of sex pheromones. EMBO Rep 14:874–883

  19. Grosse-Wilde E, Gohl T, Bouche E, Breer H, Krieger J (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 25:2364–2373

  20. Grosse-Wilde E, Stieber R, Forstner M, Krieger J, Wicher D, Hansson BS (2010) Sex-specific odorant receptors of the tobacco hornworm Manduca sexta. Front Cell Neurosci 4:22

  21. Gu SH, Yang RN, Guo MB, Wang GR, Wu KM, Guo YY, Zhou JJ, Zhang YJ (2013) Molecular identification and differential expression of sensory neuron membrane proteins in the antennae of the black cutworm moth Agrotis ipsilon. J Insect Physiol 59:430–443

  22. Guo M, Chen Q, Liu Y, Wang G, Han Z (2018) Chemoreception of mouthparts: sensilla morphology and discovery of chemosensory genes in proboscis and labial palps of adult Helicoverpa armigera (Lepidoptera: Noctuidae). Front Physiol 9:970

  23. Guo M, Krieger J, Grosse-Wilde E, Missbach C, Zhang L, Breer H (2013) Variant ionotropic receptors are expressed in olfactory sensory neurons of coeloconic sensilla on the antenna of the desert locust (Schistocerca gregaria). Int J Biol Sci 10:1–14

  24. Halty-DeLeon L, Miazzi F, Kaltofen S, Hansson BS, Wicher D (2016) The mouse receptor transporting protein RTP1S and the fly SNMP1 support the functional expression of the Drosophila odorant coreceptor Orco in mammalian culture cells. J Neurosci Methods 271:149–153

  25. Haskell PT, Mordue AJ (1969) Role of mouthpart receptors in feeding behaviour of Schistocerca gregaria. Entomol Exp Appl 12:591–610

  26. Haskell PT, Schoonhoven LM (1969) Function of certain mouth part receptors in relation to feeding in Schistocerca gregaria and Locusta migratoria migratorioides. Entomol Exp Appl 12:423–440

  27. Hassanali A, Njagi PG, Bashir MO (2005) Chemical ecology of locusts and related acridids. Annu Rev Entomol 50:223–245

  28. Iatrou K, Biessmann H (2008) Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae. Insect Biochem Mol Biol 38:268–274

  29. Jiang X, Pregitzer P, Grosse-Wilde E, Breer H, Krieger J (2016) Identification and characterization of two “sensory neuron membrane proteins” (SNMPs) of the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). J Insect Sci 16:33

  30. Jin X, Ha TS, Smith DP (2008) SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc Natl Acad Sci U S A 105:10996–11001

  31. Jin X, Zhang SG, Zhang L (2006) Expression of odorant-binding and chemosensory proteins and spatial map of chemosensilla on labial palps of Locusta migratoria (Orthoptera: Acrididae). Arthropod Struct Dev 35:47–56

  32. Jones WD, Nguyen TAT, Kloss B, Lee KJ, Vosshall LB (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr Biol 15:R119–R121

  33. Krieger J, Grosse-Wilde E, Gohl T, Breer H (2005) Candidate pheromone receptors of the silkmoth Bombyx mori. Eur J Neurosci 21:2167–2176

  34. Krieger J, Grosse-Wilde E, Gohl T, Dewer YME, Raming K, Breer H (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc Natl Acad Sci U S A 101:11845–11850

  35. Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:519–526

  36. Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446:542–546

  37. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

  38. Lebreton S, Borrero-Echeverry F, Gonzalez F, Solum M, Wallin EA, Hedenstrom E, Hansson BS, Gustavsson AL, Bengtsson M, Birgersson G, Walker WB, Dweck HKM, Becher PG, Witzgall P (2017) A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food. BMC Biol 15:88

  39. Levai O, Feistel T, Breer H, Strotmann J (2006) Cells in the vomeronasal organ express odorant receptors but project to the accessory olfactory bulb. J Comp Neurol 498:476–490

  40. Li H, Wang P, Zhang L, Xu X, Cao Z, Zhang L (2018) Expressions of olfactory proteins in locust olfactory organs and a palp odorant receptor involved in plant aldehydes detection. Front Physiol 9:663

  41. Li Z, Ni JD, Huang J, Montell C (2014) Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity. PLoS Genet 10:e1004600

  42. Liu C, Zhang J, Liu Y, Wang G, Dong S (2014) Expression of SNMP1 and SNMP2 genes in antennal sensilla of Spodoptera exigua (Hubner). Arch Insect Biochem Physiol 85:114–126

  43. Liu S, Qiao F, Liang QM, Huang YJ, Zhou WW, Gong ZJ, Cheng J, Zhu ZR (2013a) Molecular characterization of two sensory neuron membrane proteins from Chilo supressalis (Lepidoptera: Pyralidae). Ann Entomol Soc Am 106:378–384

  44. Liu S, Zhang YR, Zhou WW, Liang QM, Yuan X, Cheng J, Zhu ZR, Gong ZJ (2013b) Identification and characterization of two sensory neuron membrane proteins from Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Arch Insect Biochem Physiol 82:29–42

  45. Mordue AJ (1979) Role of the maxillary and labial palps in the feeding behavior of Schistocerca gregaria. Entomol Exp Appl 25:279–288

  46. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642

  47. Nakahara TS, Cardozo LM, Ibarra-Soria X, Bard AD, Carvalho VMA, Trintinalia GZ, Logan DW, Papes F (2016) Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status. BMC Biol 14:12

  48. Nichols Z, Vogt RG (2008) The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem Mol Biol 38:398–415

  49. Njagi PGN, Torto B (1996) Responses of nymphs of desert locust, Schistocerca gregaria to volatiles of plants used as rearing diet. Chemoecology 7:172–178

  50. Ochieng' SA, Hansson BS (1999) Responses of olfactory receptor neurones to behaviourally important odours in gregarious and solitarious desert locust, Schistocerca gregaria. Physiol Entomol 24:28–36

  51. Pener MP, Simpson SJ (2009) Locust phase polyphenism: an update. Adv Insect Physiol 36:1–272

  52. Pregitzer P, Greschista M, Breer H, Krieger J (2014) The sensory neurone membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system. Insect Mol Biol 23:733–742

  53. Pregitzer P, Jiang X, Grosse-Wilde E, Breer H, Krieger J, Fleischer J (2017) In search for pheromone receptors: certain members of the odorant receptor family in the desert locust Schistocerca gregaria (Orthoptera: Acrididae) are co-expressed with SNMP1. Int J Biol Sci 13:911–922

  54. Pregitzer P, Zielonka M, Eichhorn AS, Jiang X, Krieger J, Breer H (2019) Expression of odorant-binding proteins in mouthpart palps of the desert locust Schistocerca gregaria. Insect Mol Biol 28:264–276

  55. Roffey J, Popov G (1968) Environmental and behavioural processes in a desert locust outbreak. Nature 219:446–450

  56. Rogers ME, Krieger J, Vogt RG (2001a) Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. J Neurobiol 49:47–61

  57. Rogers ME, Steinbrecht RA, Vogt RG (2001b) Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus. Cell Tissue Res 303:433–446

  58. Rogers ME, Sun M, Lerner MR, Vogt RG (1997) Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins. J Biol Chem 272:14792–14799

  59. Ronderos DS, Lin CC, Potter CJ, Smith DP (2014) Farnesol-detecting olfactory neurons in Drosophila. J Neurosci 34:3959–3968

  60. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 101:16653–16658

  61. Seidelmann K, Luber K, Ferenz HJ (2000) Analysis of release and role of benzyl cyanide in male desert locusts, Schistocerca gregaria. J Chem Ecol 26:1897–1910

  62. Simpson SJ, Sword GA (2008) Locusts. Curr Biol 18:R364–R366

  63. Skaf R, Popov GB, Roffey J (1990) The desert locust - an international challenge. Philos Trans R Soc B 328:525–538

  64. van Huis A, Cressman K, Magor JI (2007) Preventing desert locust plagues: optimizing management interventions. Entomol Exp Appl 122:191–214

  65. Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36:497–498

  66. Winstanley C, Blaney WM (1978) Chemosensory mechanisms of locusts in relation to feeding. Entomol Exp Appl 24:750–758

  67. Zhang L, Li H, Zhang L (2017) Two olfactory pathways to detect aldehydes on locust mouthpart. Int J Biol Sci 13:759–771

Download references

Acknowledgments

The authors would like to thank Kathrin Dietze and Heidrun Froß for the excellent technical assistance. We also thank Xingcong Jiang for the technical support.

Author information

Correspondence to Jörg Fleischer.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

All applicable international, national and institutional guidelines for the care and use of animals were followed.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lemke, R., Pregitzer, P., Eichhorn, A. et al. SNMP1 and odorant receptors are co-expressed in olfactory neurons of the labial and maxillary palps from the desert locust Schistocerca gregaria (Orthoptera: Acrididae). Cell Tissue Res 379, 275–289 (2020). https://doi.org/10.1007/s00441-019-03083-x

Download citation

Keywords

  • Chemosensation
  • Insect mouthparts
  • Orco
  • Pheromone detection
  • Sensory neuron membrane protein 1