Specific transcription factors regulate the expression of Rh6 in Bactrocera minax and Bactrocera dorsalis (Diptera: Tephritidae)

Wang, Haoran; Zhang, Guijian; Wang, Yaohui; Cao, Zhen; Cao, Shuai; Wei, Bingbing; Liu, Yi; Lienard, Marjorie; Niu, Changying

doi:10.1016/j.ijbiomac.2025.141201

Article (Scientific journals)

Specific transcription factors regulate the expression of Rh6 in Bactrocera minax and Bactrocera dorsalis (Diptera: Tephritidae)

Wang, Haoran; Zhang, Guijian; Wang, Yaohui et al.

2025 • In International Journal of Biological Macromolecules, p. 141201

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https://hdl.handle.net/2268/328472

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10.1016/j.ijbiomac.2025.141201

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Abstract :

[en] Color vision is widely used by herbivorous insects to make host location. We have previously demonstrated that the long-wavelength-sensitive (LWS) opsin gene Rhodopsin 6 (Rh6) confers green preference in Bactrocera minax (a specialist) but yellow in B. dorsalis (a generalist). However, the transcriptional regulation underlying Rh6 expression and its association with color preference between these two sister species remains unclear. Here, we cloned the core promoter regions of BmRh6 and BdRh6, and identified the transcription factors (TFs) BmHmx in B. minax and BdPtx1 in B. dorsalis through bioinformatics and transcriptomic analysis. The functional impact of the two TFs on Rh6 transcription was validated using the dual luciferase reporter assays and yeast one-hybrid (Y1H) assays. RNA interference (RNAi)-mediated knockdown of the TFs resulted in significant downregulation of Rh6 expression. Furthermore, silencing of BmHmx eliminated the preference for green in B. minax, while knockdown of BdPtx1 in B. dorsalis led to the loss of yellow preference. Our results elucidate the mechanism underlying transcriptional regulation of Rh6 towards color preferences in tephritids, which also provide new insights into the links between host location and visual ecology in insects.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Wang, Haoran

Zhang, Guijian

Wang, Yaohui

Cao, Zhen

Cao, Shuai

Wei, Bingbing

Liu, Yi

Lienard, Marjorie ; Université de Liège - ULiège > Département des sciences de la vie

Niu, Changying

Language :

English

Title :

Specific transcription factors regulate the expression of Rh6 in Bactrocera minax and Bactrocera dorsalis (Diptera: Tephritidae)

Publication date :

February 2025

Journal title :

International Journal of Biological Macromolecules

ISSN :

0141-8130

eISSN :

1879-0003

Publisher :

Elsevier BV

Pages :

141201

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0141813025017507?httpAccept=text/xml

Available on ORBi :

since 18 February 2025

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Bibliography

D. Alonso San Alberto, C. Rusch, Y. Zhan, A.D. Straw, C. Montell, J.A. Riffell, The olfactory gating of visual preferences to human skin and visible spectra in mosquitoes, Nat. Commun. 13 (2022) 555, doi: https://doi.org/10.1038/s41467-022-28195-x.
Hempel de Ibarra, N., Holtze, S., Bäucker, C., Sprau, P., Vorobyev, M., The role of colour patterns for the recognition of flowers by bees. Philos. Trans. R. Soc. B, 377, 2022, 20210284, 10.1098/rstb.2021.0284.
Longden, K.D., Rogers, E.M., Nern, A., Dionne, H., Reiser, M.B., Different spectral sensitivities of ON- and OFF-motion pathways enhance the detection of approaching color objects in Drosophila. Nat. Commun., 14, 2023, 7693, 10.1038/s41467-023-43566-8.
Wu, W., Chen, Y., Yang, E., Chromatic cues to trap the oriental fruit fly, Bactrocera dorsalis. J. Insect Physiol. 53 (2007), 509–516, 10.1016/j.jinsphys.2007.02.003.
Teixeira, L., Gut, L., Isaacs, R., Response of apple maggot and cherry fruit fly (Diptera: Tephritidae) to color and contrast cues from small deposits. J. Entomol. Sci. 45 (2010), 65–74, 10.18474/0749-8004-45.2.65.
Piñero, J.C., Souder, S.K., Vargas, R.I., Vision-mediated exploitation of a novel host plant by a tephritid fruit fly. PLoS One, 12, 2017, e0174636, 10.1371/journal.pone.0174636.
Feuda, R., Marlétaz, F., Bentley, M.A., Holland, P.W.H., Conservation, duplication, and divergence of five opsin genes in insect evolution. Genome Biol. Evol. 8 (2016), 579–587, 10.1093/gbe/evw015.
van der Kooi, C.J., Stavenga, D.G., Arikawa, K., Belušič, G., Kelber, A., Evolution of insect color vision: from spectral sensitivity to visual ecology. Annu. Rev. Entomol. 66 (2021), 435–461, 10.1146/annurev-ento-061720-071644.
Ogawa, Y., Kinoshita, M., Stavenga, D.G., Arikawa, K., Sex-specific retinal pigmentation results in sexually dimorphic long-wavelength-sensitive photoreceptors in the eastern pale clouded yellow butterfly, Colias erate. J. Exp. Biol. 216 (2013), 1916–1923, 10.1242/jeb.083485.
Wernet, M.F., Perry, M.W., Desplan, C., The evolutionary diversity of insect retinal mosaics: common design principles and emerging molecular logic. Trends Genet. 31 (2015), 316–328, 10.1016/j.tig.2015.04.006.
Sharkey, C.R., Blanco, J., Leibowitz, M.M., Pinto-Benito, D., Wardill, T.J., The spectral sensitivity of Drosophila photoreceptors. Sci. Rep., 10, 2020, 18242, 10.1038/s41598-020-74742-1.
Cook, T., Pichaud, F., Sonneville, R., Papatsenko, D., Desplan, C., Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev. Cell 4 (2003), 853–864, 10.1016/s1534-5807(03)00156-4.
Rister, J., Desplan, C., The retinal mosaics of opsin expression in invertebrates and vertebrates. Dev. Neurobiol. 71 (2011), 1212–1226, 10.1002/dneu.20905.
Sandkam, B.A., Campello, L., O'Brien, C., Nandamuri, S.P., Gammerdinger, W.J., Conte, M.A., Swaroop, A., Carleton, K.L., Tbx2a modulates switching of RH2 and LWS opsin gene expression. Mol. Biol. Evol. 37 (2020), 2002–2014, 10.1093/molbev/msaa062.
Yilmaz, A., Hempel de Ibarra, N., Kelber, A., High diversity of arthropod colour vision: from genes to ecology. Philos. Trans. R. Soc. B, 377, 2022, 20210273, 10.1098/rstb.2021.0273.
Chen, Y., Desplan, C., Gene regulatory networks during the development of the Drosophila visual system. Curr. Top. Dev. Biol., 139, 2020, 10.1016/bs.ctdb.2020.02.010.
Mikeladze-Dvali, T., Wernet, M.F., Pistillo, D., Mazzoni, E.O., Teleman, A.A., Chen, Y., Cohen, S., Desplan, C., The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 122 (2005), 775–787, 10.1016/j.cell.2005.07.026.
Johnston, R.J., Otake, Y., Sood, P., Vogt, N., Behnia, R., Vasiliauskas, D., McDonald, E., Xie, B., Koenig, S., Wolf, R., Interlocked feedforward loops control cell-type-specific Rhodopsin expression in the Drosophila eye. Cell 145 (2011), 956–968, 10.1016/j.cell.2011.05.003.
Miller, A.C., Urban, E.A., Lyons, E.L., Herman, T.G., Johnston, R.J. Jr., Interdependent regulation of stereotyped and stochastic photoreceptor fates in the fly eye. Dev. Biol. 471 (2021), 89–96, 10.1016/j.ydbio.2020.12.008.
Papanicolaou, A., Schetelig, M.F., Arensburger, P., Atkinson, P.W., Benoit, J.B., Bourtzis, K., Castañera, P., Cavanaugh, J.P., Chao, H., Childers, C., Curril, I., Dinh, H., Doddapaneni, H., Dolan, A., Dugan, S., Friedrich, M., Gasperi, G., Geib, S., Georgakilas, G., Gibbs, R.A., Giers, S.D., Gomulski, L.M., González-Guzmán, M., Guillem-Amat, A., Han, Y., Hatzigeorgiou, A.G., Hernández-Crespo, P., Hughes, D.S.T., Jones, J.W., Karagkouni, D., Koskinioti, P., Lee, S.L., Malacrida, A.R., Manni, M., Mathiopoulos, K., Meccariello, A., Munoz-Torres, M., Murali, S.C., Murphy, T.D., Muzny, D.M., Oberhofer, G., Ortego, F., Paraskevopoulou, M.D., Poelchau, M., Qu, J., Reczko, M., Robertson, H.M., Rosendale, A.J., Rosselot, A.E., Saccone, G., Salvemini, M., Savini, G., Schreiner, P., Scolari, F., Siciliano, P., Sim, S.B., Tsiamis, G., Ureña, E., Vlachos, I.S., Werren, J.H., Wimmer, E.A., Worley, K.C., Zacharopoulou, A., Richards, S., Handler, A.M., The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species. Genome Biol., 17, 2016, 192, 10.1186/s13059-016-1049-2.
Sparks, M.E., Bansal, R., Benoit, J.B., Blackburn, M.B., Chao, H., Chen, M., Cheng, S., Childers, C., Dinh, H., Doddapaneni, H.V., Brown marmorated stink bug, Halyomorpha halys (Stål), genome: putative underpinnings of polyphagy, insecticide resistance potential and biology of a top worldwide pest. BMC Genomics 21 (2020), 1–26, 10.1186/s12864-020-6510-7.
Guignard, Q., Spaethe, J., Slippers, B., Strube-Bloss, M., Allison, J.D., Evidence for UV-green dichromacy in the basal hymenopteran Sirex noctilio (Siricidae). Sci. Rep., 11, 2021, 15601, 10.1038/s41598-021-95107-2.
Wang, Y., Fang, G., Xu, P., Gao, B., Liu, X., Qi, X., Zhang, G., Cao, S., Li, Z., Ren, X., Wang, H., Cao, Y., Pereira, R., Huang, Y., Niu, C., Zhan, S., Behavioral and genomic divergence between a generalist and a specialist fly. Cell Rep., 41, 2022, 111654, 10.1016/j.celrep.2022.111654.
Egri, Á., Mészáros, Á., Kriska, G., Fail, J., Dichromacy in the brown marmorated stink bug? Spectral sensitivity of the compound eyes and phototaxis of Halyomorpha halys. J. Pest Sci. 97 (2024), 657–666, 10.1007/s10340-023-01655-z.
Mahato, S., Morita, S., Tucker, A.E., Liang, X., Jackowska, M., Friedrich, M., Shiga, Y., Zelhof, A.C., Common transcriptional mechanisms for visual photoreceptor cell differentiation among Pancrustaceans. PLoS Genet., 10, 2014, e1004484, 10.1371/journal.pgen.1004484.
Perry, M., Kinoshita, M., Saldi, G., Huo, L., Arikawa, K., Desplan, C., Molecular logic behind the three-way stochastic choices that expand butterfly colour vision. Nature 535 (2016), 280–284, 10.1038/nature18616.
McCulloch, K.J., Macias-Muñoz, A., Mortazavi, A., Briscoe, A.D., Multiple mechanisms of photoreceptor spectral tuning in Heliconius butterflies. Mol. Biol. Evol., 39, 2022, 10.1093/molbev/msac067.
Liénard, M.A., Bernard, G.D., Allen, A., Lassance, J.-M., Song, S., Childers, R.R., Yu, N., Ye, D., Stephenson, A., Valencia-Montoya, W.A., The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies. Proc. Natl. Acad. Sci. USA, 118, 2021, e2008986118, 10.1073/pnas.2008986118.
Warrant, E., Somanathan, H., Colour vision in nocturnal insects. Philos. Trans. R. Soc. B, 377, 2022, 20210285, 10.1098/rstb.2021.0285.
Aluja, M., Prokopy, R.J., Host odor and visual stimulus interaction during intratree host finding behavior of Rhagoletis pomonella flies. J. Chem. Ecol. 19 (1993), 2671–2696, 10.1007/BF00980700.
Brévault, T., Quilici, S., Interaction between visual and olfactory cues during host finding in the tomato fruit fly Neoceratitis cyanescens. J. Chem. Ecol. 36 (2010), 249–259, 10.1007/s10886-010-9766-6.
Yee, W.L., Evaluation of yellow rectangle traps coated with hot melt pressure sensitive adhesive and sticky gel against Rhagoletis indifferens (Diptera: Tephritidae). J. Econ. Entomol. 104 (2011), 909–919, 10.1603/ec10327.
Chu, C., Simmons, A.M., Chen, T., Alexander, P.J., Henneberry, T., Lime green light-emitting diode equipped yellow sticky card traps for monitoring whiteflies, aphids and fungus gnats in greenhouses. Insect Sci. 11 (2004), 125–133, 10.1111/j.1744-7917.2004.tb00186.x.
Silva, D., Salamanca, J., Kyryczenko-Roth, V., Alborn, H.T., Rodriguez-Saona, C., Comparison of trap types, placement, and colors for monitoring Anthonomus musculus (Coleoptera: Curculionidae) adults in highbush blueberries. J. Insect Sci., 18, 2018, 19, 10.1093/jisesa/iey005.
Wang, Y., Andongma, A.A., Dong, Y., Chen, Z., Xu, P., Ren, X., Krosch, M.N., Clarke, A.R., Niu, C., Rh6 gene modulates the visual mechanism of host utilization in fruit fly Bactrocera minax. Pest Manag. Sci. 75 (2019), 1621–1629, 10.1002/ps.5278.
Lopez-Reyes, K., Armstrong, K.F., Van Tol, R.W., Teulon, D.A., Bok, M.J., Colour vision in thrips (Thysanoptera). Philos. Trans. R. Soc. B, 377, 2022, 20210282, 10.1098/rstb.2021.0282.
Cornelius, M.L., Duan, J.J., Messing, R.H., Visual stimuli and the response of female oriental fruit flies (Diptera: Tephritidae) to fruit-mimicking traps. J. Econ. Entomol. 92 (1999), 121–129, 10.1093/jee/92.1.121.
Lin, J., Hao, X., Yue, G., Yang, D., Lu, N., Cai, P., Ao, G., Ji, Q., Efficacy of wax-based bait stations for controlling Bactrocera dorsalis (Diptera: Tephritidae). Pest Manag. Sci. 78 (2022), 3576–3586, 10.1002/ps.7000.
Cui, Z., Si, P., Liu, L., Chen, S., Wang, Y., Li, X., Zhou, J., Zhou, Q., Push-pull strategy for integrated control of Bactrocera minax (Diptera, Tephritidae) based on olfaction and vision. J. Appl. Entomol. 146 (2022), 1243–1251, 10.1111/jen.13067.
Ren, X., Yang, Y., Guo, R., Wang, H., Qi, X., Cao, S., Lai, Y., Zhang, G., Niu, C., Yeast mediates the interspecific interaction between introduced Bactrocera dorsalis and indigenous Bactrocera minax. Pest Manag. Sci. 79 (2023), 428–436, 10.1002/ps.7211.
Li, D., Duan, S., Yang, R., Yi, S., Liu, A., Abdelnabby, H.E., Wang, M., BarH1 regulates odorant-binding proteins expression and olfactory perception of Monochamus alternatus Hope. Insect Biochem. Mol. Biol., 140, 2022, 103677, 10.1016/j.ibmb.2021.103677.
Xu, L., Qin, J., Fu, W., Wang, S., Wu, Q., Zhou, X., Crickmore, N., Guo, Z., Zhang, Y., MAP4K4 controlled transcription factor POUM1 regulates PxABCG1 expression influencing Cry1Ac resistance in Plutella xylostella (L.), Pestic. Biochem. Physiol., 182, 2022, 105053, 10.1016/j.pestbp.2022.105053.
McCulloch, K.J., Macias-Muñoz, A., Briscoe, A.D., Insect opsins and evo-devo: what have we learned in 25 years?. Philos. Trans. R. Soc. B, 377, 2022, 20210288, 10.1098/rstb.2021.0288.
Futahashi, R., Kawahara-Miki, R., Kinoshita, M., Yoshitake, K., Yajima, S., Arikawa, K., Fukatsu, T., Extraordinary diversity of visual opsin genes in dragonflies. Proc. Natl. Acad. Sci. USA 112 (2015), E1247–E1256, 10.1073/pnas.1424670112.
Lichtenstein, L., Grübel, K., Spaethe, J., Opsin expression patterns coincide with photoreceptor development during pupal development in the honey bee, Apis mellifera. BMC Dev. Biol. 18 (2018), 1–11, 10.1186/s12861-018-0162-8.
Huang, M., Meng, J., Tang, X., Shan, L., Yang, C., Zhang, C., Identification, expression analysis, and functional verification of three opsin genes related to the phototactic behaviour of Ostrinia furnacalis. Mol. Ecol., e17323, 2024, 10.1111/mec.17323.
Sondhi, Y., Ellis, E.A., Bybee, S.M., Theobald, J.C., Kawahara, A.Y., Light environment drives evolution of color vision genes in butterflies and moths. Commun. Biol., 4, 2021, 177, 10.1038/s42003-021-01688-z.
Mulhair, P.O., Crowley, L., Boyes, D.H., Lewis, O.T., Holland, P.W.H., Opsin gene duplication in Lepidoptera: retrotransposition, sex linkage, and gene expression. Mol. Biol. Evol., 40, 2023, 10.1093/molbev/msad241.
Chou, W.H., Huber, A., Bentrop, J., Schulz, S., Schwab, K., Chadwell, L.V., Paulsen, R., Britt, S.G., Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 126 (1999), 607–616, 10.1242/dev.126.4.607.
Quiquand, M., Rimesso, G., Qiao, N., Suo, S., Zhao, C., Slattery, M., White, K.P., Han, J.J., Baker, N.E., New regulators of Drosophila eye development identified from temporal transcriptome changes. Genetics, 217, 2021, 10.1093/genetics/iyab007.
Papadogiannis, V., Pennati, A., Parker, H.J., Rothbächer, U., Patthey, C., Bronner, M.E., Shimeld, S.M., Hmx gene conservation identifies the origin of vertebrate cranial ganglia. Nature 605 (2022), 701–705, 10.1038/s41586-022-04742-w.
Jiao, J., Curley, M., Graca, F.A., Robles-Murguia, M., Shirinifard, A., Finkelstein, D., Xu, B., Fan, Y., Demontis, F., Modulation of protease expression by the transcription factor Ptx1/PITX regulates protein quality control during aging. Cell Rep., 42, 2023, 111970, 10.1016/j.celrep.2022.111970.
Tran, T.Q., Kioussi, C., Pitx genes in development and disease. Cell. Mol. Life Sci. 78 (2021), 4921–4938, 10.1007/s00018-021-03833-7.
Angueyra, J.M., Kunze, V.P., Patak, L.K., Kim, H., Kindt, K., Li, W., Transcription factors underlying photoreceptor diversity. Elife, 12, 2023, e81579, 10.7554/eLife.81579.
Ordway, A.J., Helt, R.N., Johnston, R.J. Jr., Transcriptional priming and chromatin regulation during stochastic cell fate specification. Philos. Trans. R. Soc. B, 379, 2024, 20230046, 10.1098/rstb.2023.0046.
Song, J., VanBuskirk, J.A., Merbs, S.L., Regulation of opsin gene expression by DNA methylation and histone acetylation. Int. J. Mol. Sci., 23, 2022, 1408, 10.3390/ijms23031408.
Meccariello, A., Hou, S., Davydova, S., Fawcett, J.D., Siddall, A., Leftwich, P.T., Krsticevic, F., Papathanos, P.A., Windbichler, N., Gene drive and genetic sex conversion in the global agricultural pest Ceratitis capitata. Nat. Commun., 15, 2024, 372, 10.1038/s41467-023-44399-1.