Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-29T15:24:50.794Z Has data issue: false hasContentIssue false

The melanin pigment gene black mediates body pigmentation and courtship behaviour in the German cockroach Blattella germanica

Published online by Cambridge University Press:  16 April 2024

Lang-Lang Gong
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
Yun-Feng Ma
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
Meng-Qi Zhang
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
Hong-Yan Feng
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
Yang-Yuntao Zhou
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
Ya-Qin Zhao
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
J. Joe Hull
Affiliation:
USDA-ARS Arid Land Agricultural Research Center, Maricopa AZ, 85138, USA
Youssef Dewer
Affiliation:
Phytotoxicity Research Department, Central Agricultural Pesticide Laboratory, Agricultural Research Center, 7 Nadi El-Seid Street, Dokki 12618, Giza, Egypt
Ming He*
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
Peng He*
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, PR China
*
Corresponding authors: Peng He; Email: phe1@gzu.edu.cn; Ming He; Email: hmher@126.com
Corresponding authors: Peng He; Email: phe1@gzu.edu.cn; Ming He; Email: hmher@126.com

Abstract

Genes involved in melanin production directly impact insect pigmentation and can affect diverse physiology and behaviours. The role these genes have on sex behaviour, however, is unclear. In the present study, the crucial melanin pigment gene black was functionally characterised in an urban pest, the German cockroach, Blattella germanica. RNAi knockdown of B. germanica black (Bgblack) had no effect on survival, but did result in black pigmentation of the thoraxes, abdomens, heads, wings, legs, antennae, and cerci due to cuticular accumulation of melanin. Sex-specific variation in the pigmentation pattern was apparent, with females exhibiting darker coloration on the abdomen and thorax than males. Bgblack knockdown also resulted in wing deformation and negatively impacted the contact sex pheromone-based courtship behaviour of males. This study provides evidence for black function in multiple aspects of B. germanica biology and opens new avenues of exploration for novel pest control strategies.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Lead contact.

References

Abebe, A, Zheng, D, Evans, J and Sugumaran, M (2010) Reexamination of the mechanisms of oxidative transformation of the insect cuticular sclerotizing precursor, 1,2–dehydro-N-acetyldopamine. Insect Biochemistry and Molecular Biology 40, 650659.CrossRefGoogle ScholarPubMed
Andersen, SO (2010) Insect cuticular sclerotization: a review. Insect Biochemistry and Molecular Biology 40, 166178.CrossRefGoogle ScholarPubMed
Andretic, R, van Swinderen, B and Greenspan, RJ (2005) Dopaminergic modulation of arousal in Drosophila. Current Biology 15, 11651175.CrossRefGoogle ScholarPubMed
Angelini, DR, Liu, PZ, Hughes, CL and Kaufman, TC (2005) Hox gene function and interaction in the milkweed bug Oncopeltus fasciatus (Hemiptera). Developmental Biology 287, 440455.CrossRefGoogle ScholarPubMed
Arakane, Y, Lomakin, J, Beeman, RW, Muthukrishnan, S, Gehrke, SH, Kanost, MR and Kramer, KJ (2009) Molecular and functional analyses of amino acid decarboxylases involved in cuticle tanning in Tribolium castaneum. Journal of Biological Chemistry 284, 1658416594.CrossRefGoogle ScholarPubMed
Auer, TO and Benton, R (2016) Sexual circuitry in Drosophila. Current Opinion in Neurobiology 38, 1826.CrossRefGoogle ScholarPubMed
Aust, S, Brüsselbach, F, Pütz, S and Hovemann, BT (2010) Alternative tasks of Drosophila tan in neurotransmitter recycling versus cuticle sclerotization disclosed by kinetic properties. Journal of Biological Chemistry 285, 2074020747.CrossRefGoogle Scholar
Bai, TT, Pei, XJ, Liu, TX, Fan, YL and Zhang, SZ (2022) Melanin synthesis genes BgTH and BgDdc affect body color and cuticle permeability in Blattella germanica. Insect Science 29, 15521568.CrossRefGoogle ScholarPubMed
Barek, H, Sugumaran, M, Ito, S and Wakamatsu, K (2018a) Insect cuticular melanins are distinctly different from those of mammalian epidermal melanins. Pigment Cell & Melanoma Research 31, 384392.Google ScholarPubMed
Barek, H, Veraksa, A and Sugumaran, M (2018b) Drosophila melanogaster has the enzymatic machinery to make the melanic component of neuromelanin. Pigment Cell & Melanoma Research 31, 683692.CrossRefGoogle ScholarPubMed
Brent, CS, Heu, CC, Gross, RJ, Fan, B, Langhorst, D and Hull, JJ (2022) RNAi-Mediated manipulation of cuticle coloration genes in Lygus hesperus knight (Hemiptera: Miridae). Insects 13, 986.CrossRefGoogle ScholarPubMed
Carroll, SB (2005) Evolution at two levels: on genes and form. PLoS Biology 3, e245.CrossRefGoogle ScholarPubMed
Chen, P, Tong, XL, Li, DD, Fu, MY, He, SZ, Hu, H, Xiang, ZH, Lu, C and Dai, FY (2013) Antennapedia is involved in the development of thoracic legs and segmentation in the silkworm, Bombyx mori. Heredity (Edinb) 111, 182188.Google ScholarPubMed
Chen, EH, Hou, QL, Wei, DD, Dou, W, Liu, Z, Yang, PJ, Smagghe, G and Wang, JJ (2018) Tyrosine hydroxylase coordinates larval-pupal tanning and immunity in oriental fruit fly (Bactrocera dorsalis). Pest Management Science 74, 569578.CrossRefGoogle ScholarPubMed
Czapla, TH, Hopkins, TL and Kramer, KJ (1990) Catecholamines and related o-diphenols in cockroach hemolymph and cuticle during sclerotization and melanization: comparative studies on the order Dictyoptera. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 160, 175181.CrossRefGoogle ScholarPubMed
Dai, F, Qiao, L, Cao, C, Liu, X, Tong, X, He, S, Hu, H, Zhang, L, Wu, S, Tan, D, Xiang, Z and Lu, C (2015) Aspartate decarboxylase is required for a normal pupa pigmentation pattern in the silkworm, Bombyx mori. Scientific Reports 5, 10885.CrossRefGoogle ScholarPubMed
Deal, SL, Bei, D, Gibson, SB, Delgado-Seo, H, Fujita, Y, Wilwayco, K, Seto, ES and Yamamoto, S (2023) RNAi-based screen for cuticle pigmentation in Drosophila melanogaster reveals novel regulators of brain dopamine. bioRxiv, 2023.2007.2020.549932. https://doi.org/10.1101/2023.07.20.549932Google Scholar
Drapeau, MD, Radovic, A, Wittkopp, PJ and Long, AD (2003) A gene necessary for normal male courtship, yellow, acts downstream of fruitless in the Drosophila melanogaster larval brain. Journal of Neurobiology 55, 5372.CrossRefGoogle ScholarPubMed
Drapeau, MD, Cyran, SA, Viering, MM, Geyer, PK and Long, AD (2006) A cis-regulatory sequence within the yellow locus of Drosophila melanogaster required for normal male mating success. Genetics 172, 10091030.CrossRefGoogle ScholarPubMed
Eliyahu, D, Mori, K, Takikawa, H, Leal, WS and Schal, C (2004) Behavioral activity of stereoisomers and a new component of the contact sex pheromone of female German cockroach, Blattella germanica. Journal of Chemical Ecology 30, 18391848.CrossRefGoogle Scholar
Eliyahu, D, Nojima, S, Capracotta, SS, Comins, DL and Schal, C (2008) Identification of cuticular lipids eliciting interspecific courtship in the German cockroach, Blattella germanica. Naturwissenschaften 95, 403412.CrossRefGoogle ScholarPubMed
Fang, C, Xin, Y, Sun, T, Monteiro, A, Ye, Z, Dai, F, Lu, C and Tong, X (2022) The Hox gene Antennapedia is essential for wing development in insects. Development (Cambridge, England) 149, dev199841.CrossRefGoogle ScholarPubMed
Fuchs, S, Behrends, V, Bundy, JG, Crisanti, A and Nolan, T (2014) Phenylalanine metabolism regulates reproduction and parasite melanization in the malaria mosquito. PLoS One 9, e84865.CrossRefGoogle ScholarPubMed
Fukuda, S and Onishi, E (1971) Transplantation in relation to pigment formation of the integument in the larvae of the swallowtail, Papilio xuthus L. Development Growth & Differentiation 13, 279283.CrossRefGoogle ScholarPubMed
Gibert, JM, Mouchel-Vielh, E, De Castro, S and Peronnet, F (2016) Phenotypic plasticity through transcriptional regulation of the evolutionary hotspot gene tan in drosophila melanogaster. PLoS Genetics 12, e1006218.CrossRefGoogle Scholar
Gorman, MJ and Arakane, Y (2010) Tyrosine hydroxylase is required for cuticle sclerotization and pigmentation in Tribolium castaneum. Insect Biochemistry and Molecular Biology 40, 267273.CrossRefGoogle ScholarPubMed
Gorman, MJ, An, C and Kanost, MR (2007) Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochemistry and Molecular Biology 37, 13271337.CrossRefGoogle ScholarPubMed
Guo, H, Long, GJ, Liu, XZ, Ma, YF, Zhang, MQ, Gong, LL, Dewer, Y, Hull, JJ, Wang, MM, Wang, Q, He, M and He, P (2023) Functional characterization of tyrosine melanin genes in the white-backed planthopper and utilization of a spray-based nanoparticle-wrapped dsRNA technique for pest control. International Journal of Biological Macromolecules 230, 123123.CrossRefGoogle ScholarPubMed
Hamilton, JA, Wada-Katsumata, A, Ko, A and Schal, C (2021) Effects of novaluron ingestion and topical application on German cockroach (Blattella germanica) development and reproduction. Pest Management Science 77, 877885.CrossRefGoogle Scholar
Harrison, MC, Jongepier, E, Robertson, HM, Arning, N, Bitard-Feildel, T, Chao, H, Childers, CP, Dinh, H, Doddapaneni, H, Dugan, S, Gowin, J, Greiner, C, Han, Y, Hu, H, Hughes, DST, Huylmans, AK, Kemena, C, Kremer, LPM, Lee, SL, Lopez-Ezquerra, A, Mallet, L, Monroy-Kuhn, JM, Moser, A, Murali, SC, Muzny, DM, Otani, S, Piulachs, MD, Poelchau, M, Qu, J, Schaub, F, Wada-Katsumata, A, Worley, KC, Xie, Q, Ylla, G, Poulsen, M, Gibbs, RA, Schal, C, Richards, S, Belles, X, Korb, J and Bornberg-Bauer, E (2018) Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology & Evolution 2, 557566.CrossRefGoogle ScholarPubMed
Hill, HZ (1992) The function of melanin or six blind people examine an elephant. Bioessays 14, 4956.CrossRefGoogle ScholarPubMed
Hiragaki, S, Suzuki, T, Mohamed, AA and Takeda, M (2015) Structures and functions of insect arylalkylamine N-acetyltransferase (iaaNAT); a key enzyme for physiological and behavioral switch in arthropods. Frontiers in Physiology 6, 113.CrossRefGoogle ScholarPubMed
Huang, J, Zhang, Z, Feng, W, Zhao, Y, Aldanondo, A, de Brito Sanchez, MG, Paoli, M, Rolland, A, Li, Z, Nie, H, Lin, Y, Zhang, S, Giurfa, M and Su, S (2022) Food wanting is mediated by transient activation of dopaminergic signaling in the honey bee brain. Science (New York, N.Y.) 376, 508512.CrossRefGoogle ScholarPubMed
Ito, S (2003) The IFPCS presidential lecture: a chemist's view of melanogenesis. Pigment Cell Research 16, 230236.CrossRefGoogle ScholarPubMed
Ito, S and Wakamatsu, K (2003) Quantitative analysis of eumelanin and pheomelanin in humans, mice, and other animals: a comparative review. Pigment Cell Research 16, 523531.CrossRefGoogle ScholarPubMed
Ito, S and Wakamatsu, K (2008) Chemistry of mixed melanogenesis--pivotal roles of dopaquinone. Photochemistry and Photobiology 84, 582592.CrossRefGoogle ScholarPubMed
Ito, S, Wakamatsu, K and Ozeki, H (2000) Chemical analysis of melanins and its application to the study of the regulation of melanogenesis. Pigment Cell Research 13(Suppl 8), 103109.CrossRefGoogle Scholar
Ito, K, Katsuma, S, Yamamoto, K, Kadono-Okuda, K, Mita, K and Shimada, T (2010) Yellow-e determines the color pattern of larval head and tail spots of the silkworm Bombyx mori. Journal of Biological Chemistry 285, 56245629.CrossRefGoogle ScholarPubMed
Jeong, S, Rokas, A and Carroll, SB (2006) Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125, 13871399.CrossRefGoogle ScholarPubMed
Katoh, K, Rozewicki, J and Yamada, KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 11601166.Google ScholarPubMed
Konopka, RJ (1972) Abnormal concentrations of dopamine in a Drosophila mutant. Nature 239, 281282.CrossRefGoogle Scholar
Le Moëne, O and Ågmo, A (2018) The neuroendocrinology of sexual attraction. Frontiers in Neuroendocrinology 51, 4667.CrossRefGoogle ScholarPubMed
Lemonds, TR, Liu, J and Popadić, A (2016) The contribution of the melanin pathway to overall body pigmentation during ontogenesis of Periplaneta americana. Insect Science 23, 513519.CrossRefGoogle Scholar
Li, C, Zhu, H, Li, C, Qian, H, Yao, W and Guo, Y (2021) The present situation of pesticide residues in China and their removal and transformation during food processing. Food Chemistry 354, 129552.CrossRefGoogle Scholar
Liu, T, Dartevelle, L, Yuan, C, Wei, H, Wang, Y, Ferveur, JF and Guo, A (2008) Increased dopamine level enhances male-male courtship in Drosophila. Journal of Neuroscience 28, 55395546.CrossRefGoogle ScholarPubMed
Liu, J, Lemonds, TR and Popadić, A (2014) The genetic control of aposematic black pigmentation in hemimetabolous insects: insights from Oncopeltus fasciatus. Evolution & Development 16, 270277.CrossRefGoogle ScholarPubMed
Liu, J, Lemonds, TR, Marden, JH and Popadić, A (2016) A pathway analysis of melanin patterning in a hemimetabolous insect. Genetics 203, 403413.CrossRefGoogle Scholar
Liu, Y, Ramos-Womack, M, Han, C, Reilly, P, Brackett, KL, Rogers, W, Williams, TM, Andolfatto, P, Stern, DL and Rebeiz, M (2019) Changes throughout a genetic network mask the contribution of Hox gene evolution. Current Biology 29, 21572166.e2156.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif.) 25, 402408.CrossRefGoogle ScholarPubMed
Ma, YF, Gong, LL, Zhang, MQ, Liu, XZ, Guo, H, Hull, JJ, Long, GJ, Wang, H, Dewer, Y, Zhang, F, He, M and He, P (2023) Two antenna-enriched carboxylesterases mediate olfactory responses and degradation of ester volatiles in the German cockroach Blattella germanica. Journal of Agricultural and Food Chemistry 71, 47894801.CrossRefGoogle ScholarPubMed
McPherson, S, Wada-Katsumata, A, Hatano, E, Silverman, J and Schal, C (2022) Nutritional condition affects tergal gland secretion and courtship success of male cockroaches. PLoS One 17, e0271344.CrossRefGoogle ScholarPubMed
Mehere, P, Han, Q, Christensen, BM and Li, J (2011) Identification and characterization of two arylalkylamine N-acetyltransferases in the yellow fever mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology 41, 707714.CrossRefGoogle ScholarPubMed
Mei, LC, Chen, HM, Dong, AY, Huang, GY, Liu, YW, Zhang, X, Wang, W, Hao, GF and Yang, GF (2022) Pesticide informatics platform (PIP): an international platform for pesticide discovery, residue, and risk evaluation. Journal of Agricultural and Food Chemistry 70, 66176623.CrossRefGoogle ScholarPubMed
Mun, S, Mi, YN, Kramer, KJ, Muthukrishnan, S, Arakane, YJIB and Biology, M (2019) Gene functions in adult cuticle pigmentation of the yellow mealworm. Tenebrio Molitor 117, 103291.Google ScholarPubMed
Nappi, AJ and Christensen, BM (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology 35, 443459.CrossRefGoogle ScholarPubMed
Naysmith, L, Waterston, K, Ha, T, Flanagan, N, Bisset, Y, Ray, A, Wakamatsu, K, Ito, S and Rees, JL (2004) Quantitative measures of the effect of the melanocortin 1 receptor on human pigmentary status. Journal of Investigative Dermatology 122, 423428.CrossRefGoogle ScholarPubMed
Neckameyer, WS (1998) Dopamine modulates female sexual receptivity in Drosophila melanogaster. Journal of Neurogenetics 12, 101114.CrossRefGoogle ScholarPubMed
Noh, MY, Koo, B, Kramer, KJ, Muthukrishnan, S and Arakane, Y (2016a) Arylalkylamine N-acetyltransferase 1 gene (TcAANAT1) is required for cuticle morphology and pigmentation of the adult red flour beetle, Tribolium castaneum. Insect Biochemistry and Molecular Biology 79, 119129.CrossRefGoogle ScholarPubMed
Noh, MY, Muthukrishnan, S, Kramer, KJ and Arakane, Y (2016b) Cuticle formation and pigmentation in beetles. Current Opinion in insect Science 17, 19.CrossRefGoogle ScholarPubMed
Noh, MY, Mun, S, Kramer, KJ, Muthukrishnan, S and Arakane, Y (2021) Yellow-y functions in Egg melanization and chorion morphology of the Asian tiger mosquito, Aedes albopictus. Frontiers in Cell and Developmental Biology 9, 769788.CrossRefGoogle ScholarPubMed
Pan, XY and Zhang, FJBC (2019) Advances in biological control of the German cockroach, Blattella germanica (L.). Biological Control 142, 104104.CrossRefGoogle Scholar
Phillips, AM, Smart, R, Strauss, R, Brembs, B and Kelly, LE (2005) The Drosophila black enigma: the molecular and behavioural characterization of the black1 mutant allele. Gene 351, 131142.CrossRefGoogle ScholarPubMed
Popadić, A and Tsitlakidou, D (2021) Regional patterning and regulation of melanin pigmentation in insects. Current Opinion in Genetics & Development 69, 163170.CrossRefGoogle ScholarPubMed
Prota, G (1995) The chemistry of melanins and melanogenesis. Fortschritte der Chemie Organischer Naturstoffe 64, 93148.Google ScholarPubMed
Richardt, A, Kemme, T, Wagner, S, Schwarzer, D, Marahiel, MA and Hovemann, BT (2003) Ebony, a novel nonribosomal peptide synthetase for beta-alanine conjugation with biogenic amines in Drosophila. Journal of Biological Chemistry 278, 4116041166.CrossRefGoogle ScholarPubMed
Ryan, MJ (2021) Darwin, sexual selection, and the brain. Proceedings of the National Academy of Sciences of the United States of America 118, e2008194118.CrossRefGoogle ScholarPubMed
Saedi, S, Khoradmehr, A, Mohammad Reza, JS and Tamadon, A (2018) The role of neuropeptides and neurotransmitters on kisspeptin/kiss1r-signaling in female reproduction. Journal of Chemical Neuroanatomy 92, 7182.CrossRefGoogle ScholarPubMed
Shamim, G, Ranjan, SK, Pandey, DM and Ramani, RJEJoE (2014) Biochemistry and biosynthesis of insect pigments. European Journal of Entomology 111, 149164.CrossRefGoogle Scholar
Shimomura, K, Ishii, D and Nojima, S (2019) Behavioral and morphological studies of the membranous tergal structure of male Blattella germanica (Blattodea: Ectobiidae) during courtship. Journal of Insect Science 19, 14.CrossRefGoogle Scholar
Söderhäll, K and Cerenius, L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 2328.CrossRefGoogle ScholarPubMed
Sterkel, M, Ons, S and Oliveira, PL (2019) DOPA decarboxylase is essential for cuticle tanning in Rhodnius prolixus (Hemiptera: Reduviidae), affecting ecdysis, survival and reproduction. Insect Biochemistry and Molecular Biology 108, 2431.CrossRefGoogle ScholarPubMed
Suderman, RJ, Dittmer, NT, Kanost, MR and Kramer, KJ (2006) Model reactions for insect cuticle sclerotization: cross-linking of recombinant cuticular proteins upon their laccase-catalyzed oxidative conjugation with catechols. Insect Biochemistry and Molecular Biology 36, 353365.CrossRefGoogle ScholarPubMed
Sugumaran, M (2016) Reactivities of quinone methides versus o-Quinones in catecholamine metabolism and eumelanin biosynthesis. International Journal of Molecular Sciences 17, 1576. https://doi.org/10.3390/ijms17091576CrossRefGoogle ScholarPubMed
Sugumaran, M and Barek, H (2016) Critical analysis of the melanogenic pathway in insects and higher animals. International Journal of Molecular Sciences 17, 1753. https://doi.org/10.3390/ijms17101753CrossRefGoogle ScholarPubMed
Thody, AJ, Higgins, EM, Wakamatsu, K, Ito, S, Burchill, SA and Marks, JM (1991) Pheomelanin as well as eumelanin is present in human epidermis. Journal of Investigative Dermatology 97, 340344.CrossRefGoogle ScholarPubMed
True, JR, Yeh, SD, Hovemann, BT, Kemme, T, Meinertzhagen, IA, Edwards, TN, Liou, SR, Han, Q and Li, J (2005) Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genetics 1, e63.CrossRefGoogle ScholarPubMed
Wada-Katsumata, A and Schal, C (2019) Antennal grooming facilitates courtship performance in a group-living insect, the German cockroach Blattella germanica. Scientific Reports 9, 2942.CrossRefGoogle Scholar
Wan, C, Hao, Z and Feng, X (2016) Structures, properties, and energy-storage mechanisms of the semi-lunar process cuticles in locusts. Scientific Reports 6, 35219.CrossRefGoogle ScholarPubMed
Wang, H, Ma, YF, Wang, MM, Chen, GL, Dewer, Y, He, M, Zhang, F, Yang, YF, Liu, JF and He, P (2020) Expression, affinity, and functional characterization of the specific binding of Two putative pheromone-binding proteins in the omnivorous German cockroach Blattella germanica. Journal of Agricultural and Food Chemistry 68, 1357313583.CrossRefGoogle ScholarPubMed
Whitten, MMA and Coates, CJ (2017) Re-evaluation of insect melanogenesis research: views from the dark side. Pigment Cell & Melanoma Research 30, 386401.CrossRefGoogle ScholarPubMed
Wittkopp, PJ and Beldade, P (2009) Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Seminars in Cell & Developmental Biology 20, 6571.CrossRefGoogle ScholarPubMed
Wright, TR (1987) The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Advances in Genetics 24, 127222.CrossRefGoogle ScholarPubMed
Wu, X and Appel, AG (2017) Insecticide resistance of several field-collected German cockroach (Dictyoptera: Blattellidae) strains. Journal of Economic Entomology 110, 12031209.CrossRefGoogle ScholarPubMed
Yamamoto, S and Seto, ES (2014) Dopamine dynamics and signaling in Drosophila: an overview of genes, drugs and behavioral paradigms. Experimental Animals 63, 107119.CrossRefGoogle ScholarPubMed
Ze, LJ, Jin, L and Li, GQ (2022) Silencing of Adc and ebony causes abnormal darkening of cuticle in Henosepilachna vigintioctopunctata. Frontiers in Physiology 13, 829675.CrossRefGoogle ScholarPubMed
Zhang, SX, Rogulja, D and Crickmore, MA (2016) Dopaminergic circuitry underlying mating drive. Neuron 91, 168181.CrossRefGoogle ScholarPubMed
Zhang, F, Sun, XX, Zhang, XC, Zhang, S, Lu, J, Xia, YM, Huang, YH and Wang, XJ (2018) The interactions between gut microbiota and entomopathogenic fungi: a potential approach for biological control of Blattella germanica (L.). Pest Management Science 74, 438447.CrossRefGoogle ScholarPubMed
Zhu, S, Liu, Y, Liao, M, Yang, Y, Bai, Y, Li, N, Li, S, Luan, Y and Chen, N (2021) Evaluation of reference genes for transcriptional profiling in two cockroach models. Genes (Basel) 12, 1880.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gong et al. supplementary material 1

Gong et al. supplementary material
Download Gong et al. supplementary material 1(File)
File 20.1 KB
Supplementary material: File

Gong et al. supplementary material 2

Gong et al. supplementary material
Download Gong et al. supplementary material 2(File)
File 16.3 KB
Supplementary material: File

Gong et al. supplementary material 3

Gong et al. supplementary material
Download Gong et al. supplementary material 3(File)
File 25.3 MB
Supplementary material: File

Gong et al. supplementary material 4

Gong et al. supplementary material
Download Gong et al. supplementary material 4(File)
File 25.3 MB
Supplementary material: File

Gong et al. supplementary material 5

Gong et al. supplementary material
Download Gong et al. supplementary material 5(File)
File 25.3 MB
Supplementary material: File

Gong et al. supplementary material 6

Gong et al. supplementary material
Download Gong et al. supplementary material 6(File)
File 25.3 MB