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

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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.

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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

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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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.

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Correspondence to Jörg Fleischer.

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Lemke, RS., Pregitzer, P., Eichhorn, AS. 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

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