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Imaginal disc growth factor maintains cuticle structure and controls melanization in the spot pattern formation of Bombyx mori


Autoři: Yun Gao aff001;  Yun-Cai Liu aff001;  Shun-Ze Jia aff001;  Yan-Ting Liang aff001;  Yu Tang aff001;  Yu-Song Xu aff001;  Hideki Kawasak aff002;  Hua-Bing Wang aff001;  Hideki Kawasaki aff002
Působiště autorů: College of Animal Sciences, Zhejiang University, Hangzhou, China aff001;  Faculty of Agriculture, Takasaki University of Health and Welfare, Gunma, Japan aff002
Vyšlo v časopise: Imaginal disc growth factor maintains cuticle structure and controls melanization in the spot pattern formation of Bombyx mori. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1008980
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008980

Souhrn

The complex stripes and patterns of insects play key roles in behavior and ecology. However, the fine-scale regulation mechanisms underlying pigment formation and morphological divergence remain largely unelucidated. Here we demonstrated that imaginal disc growth factor (IDGF) maintains cuticle structure and controls melanization in spot pattern formation of Bombyx mori. Moreover, our knockout experiments showed that IDGF is suggested to impact the expression levels of the ecdysone inducible transcription factor E75A and pleiotropic factors apt-like and Toll8/spz3, to further control the melanin metabolism. Furthermore, the untargeted metabolomics analyses revealed that BmIDGF significantly affected critical metabolites involved in phenylalanine, beta-alanine, purine, and tyrosine metabolism pathways. Our findings highlighted not only the universal function of IDGF to the maintenance of normal cuticle structure but also an underexplored space in the gene function affecting melanin formation. Therefore, this study furthers our understanding of insect pigment metabolism and melanin pattern polymorphisms.

Klíčová slova:

Insects – Larvae – Melanin – Metabolic pathways – Metabolites – Metabolomics – Molting – Purine metabolism


Zdroje

1. Kronforst MR, Young LG, Kapan DD, Camille MN, Neill RJ, Gilbert LE. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc Natl Acad Sci USA. 2006;103(17):6575–6580. doi: 10.1073/pnas.0509685103 16611733

2. Wittkopp PJ, Stewart EE, Arnold LL, Neidert AH, Haerum BK, Thompson EM, et al. Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science. 2009;326(5952):540–544. doi: 10.1126/science.1176980 19900891

3. Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, et al. Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science. 2011;333(6046):1137–1141. doi: 10.1126/science.1208227 21778360

4. Rogers WA, Salomone JR, Tacy DJ, Camino EM, Davis KA, Rebeiz M, et al. Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity. PLoS Genet. 2013;9(8):e1003740. doi: 10.1371/journal.pgen.1003740 24009528

5. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB. Stepwise Modification of a modular enhancer underlies adaptation in a Drosophila population. Science. 2009; 326(5960):1663–7. doi: 10.1126/science.1178357 20019281

6. Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci USA. 2012;109(31):12632–12637. doi: 10.1073/pnas.1204800109 22802635

7. Werner T, Koshikawa S, Williams TM, Carroll SB. Generation of a novel wing colour pattern by the Wingless morphogen. Nature. 2010;464(7292):1143–1148. doi: 10.1038/nature08896 20376004

8. Yamaguchi J, Banno Y, Mita K, Yamamoto K, Ando T, Fujiwara H. Periodic Wnt1 expression in response to ecdysteroid generates twin-spot markings on caterpillars. Nat Commun. 2013;4(5):1857–1865. doi: 10.1038/ncomms2778 23673642

9. Yoda S. The transcription factor Apontic-like controls diverse coloration pattern in caterpillars. Nat Commun. 2015;4(5):4936–4936. doi: 10.1038/ncomms5936 25233442

10. Wittkopp PJ, Carroll SB, Kopp A. Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet. 2003;19(9):495–504. doi: 10.1016/S0168-9525(03)00194-X 12957543

11. Kondo Y, Yoda S, Mizoguchi T, Ando T, Yamaguchi J, Yamamoto K, et al. Toll ligand Spatzle3 controls melanization in the stripe pattern formation in caterpillars. Proc Natl Acad Sci USA. 2017;114(31):8336–8341. doi: 10.1073/pnas.1707896114 28716921

12. Yu HS, Shen YH, Yuan GX, Hu YG, Xu HE, Xiang ZH, et al. Evidence of selection at melanin synthesis pathway loci during silkworm domestication. Mol biol evol. 2011; 28 (6):1785–1799. doi: 10.1093/molbev/msr002 21212153

13. Caro T, Izzo A, Reiner RC, Walker H, Stankowich T. The function of zebra stripes. Nat Commun. 2014;5(4):3535–3544. doi: 10.1038/ncomms4535 24691390

14. Mallarino R, Henegar C, Mirasierra M, Manceau M, Schradin C, Vallejo M, et al. Developmental mechanisms of stripe patterns in rodents. Nature. 2016; 539(7630): 518–523. doi: 10.1038/nature20109 27806375

15. Fujiwara H, Nishikawa H. Functional analysis of genes involved in color pattern formation in Lepidoptera. Curr Opin Insect Sci. 2016;17:16–23. doi: 10.1016/j.cois.2016.05.015 27720069

16. Futahashi R, Fujiwara H. Regulation of 20-hydroxyecdysone on the larval pigmentation and the expression of melanin synthesis enzymes and yellow gene of the swallowtail butterfly, Papilio xuthus. Insect Biochem Mol Biol. 2007;37(8):855–864. doi: 10.1016/j.ibmb.2007.02.014 17628284

17. Hiruma K, Riddiford LM. The molecular mechanisms of cuticular melanization: The ecdysone cascade leading to dopa decarboxylase expression in Manduca sexta. Insect Biochem Mol Biol.2009;39(4):245–253. doi: 10.1016/j.ibmb.2009.01.008 19552890

18. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, et al. A Draft Sequence for the Genome of the Domesticated Silkworm (Bombyx mori). Science. 2004;306(5703):1937–1940. doi: 10.1126/science.1102210 15591204

19. Consortium T. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol. 2008;38(12):1036–1045. doi: 10.1016/j.ibmb.2008.11.004 19121390

20. Yamamoto K, Nohata J, Kadono-Okuda K, Narukawa J. A BAC-based integrated linkage map of the silkworm Bombyx mori. Genome Biology. 2008;9(1):R21. doi: 10.1186/gb-2008-9-1-r21 18226216

21. Meng Y, Katsuma S, Daimon T, Banno Y, Uchino K, Sezutsu H, et al. The Silkworm mutant lemon (lemon lethal) is a potential insect model for human sepiapterin reductase deficiency. J Biol Chem. 2009;284(17):11698–11705. doi: 10.1074/jbc.M900485200 19246455

22. Kidokoro K, Ohnuma A, Mita K, Noda H, Kobayashi I, Tamura T, et al. Repression of tyrosine hydroxylase is responsible for the sex-linked chocolate mutation of the silkworm, Bombyx mori. Proc Natl Acad Sci USA. 2010;107(29):12980–12985. doi: 10.1073/pnas.1001725107 20615980

23. Liu W, Gray S, Huo Y, li L, Wei T, Wang X. Proteomic analysis of interaction between a plant virus and its vector insect reveals new functions of hemipteran cuticular protein. Molecular & Cellular Proteomics. 2015;14(8):2229–2242. doi: 10.1074/mcp.M114.046763 26091699

24. Moussian B. Recent advances in understanding mechanisms of insect cuticle differentiation. Insect Biochem Mol Biol. 2010;40(5):363–375. doi: 10.1016/j.ibmb.2010.03.003 20347980

25. Xiong G, Tong XL, Gai TT, Li CL, Qiao L, Monteiro A et al. Body shape and coloration of silkworm larvae are influenced by a novel cuticular protein. Genetics. 2017; 207(3): 1053–1066. doi: 10.1534/genetics.117.300300 28923848

26. Lu JB, Luo XM, Zhang XY, Pan PL, Zhang CX. An ungrouped cuticular protein is essential for normal endocuticle formation in the brown planthopper. Insect Biochem Mol Biol.2018;100:1–9. doi: 10.1016/j.ibmb.2018.06.001 29885440

27. Pesch Y-Y, Riedel D, Patil KR, Loch G, Behr M. Chitinases and Imaginal disc growth factors organize the extracellular matrix formation at barrier tissues in insects. Sci Rep. 2015;6(1):18340–18353. doi: 10.1038/srep18340 26838602

28. Broz V, Kucerova L, Rouhova L, Fleischmannova J, Zurovec M. Drosophila imaginal disc growth factor 2 is a trophic factor involved in energy balance, detoxification, and innate immunity. Sci Rep. 2017;7(6):43273–43287. doi: 10.1038/srep43273 28230183

29. Gu X, Li Z, Su Y, Zhao Y, Liu L. Imaginal disc growth factor 4 regulates development and temperature adaptation in Bactrocera dorsalis. Sci Rep. 2019;9(1):931–940. doi: 10.1038/s41598-018-37414-9 30700762

30. Zurovcova M, Benes V, Zurovec M, Kucerova L. Expansion of imaginal disc growth factor gene family in diptera reflects the evolution of novel functions. Insects. 2019;10(10):365. doi: 10.3390/insects10100365 31635152

31. Zhang J, Iwai S, Tsugehara T, Takeda M. MbIDGF, a novel member of the imaginal disc growth factor family in Mamestra brassicae, stimulates cell proliferation in two lepidopteran cell lines without insulin. Insect Biochem Mol Biol. 2006;36(7):536–546. doi: 10.1016/j.ibmb.2006.04.002 16835019

32. Wang HB, Sakudoh T, Kawasaki H, Iwanaga M, Araki K, Fujimoto H, et al. Purification and expression analysis of imaginal disc growth factor in the silkworm, Bombyx mori. J Insect Physiol. 2009;55(11):1065–1071. doi: 10.1016/j.jinsphys.2009.08.001 19682451

33. Qu M, Ma L, Chen P, Yang Q. Proteomic analysis of insect molting fluid with a focus on enzymes involved in chitin degradation. J Proteome Res. 2014;13(6):2931–2940. doi: 10.1021/pr5000957 24779478

34. Varela PF, Llera AS, Mariuzza RA, Tormo J. Crystal Structure of Imaginal Disc Growth Factor-2: a member of a new family of growth-promoting glycopromteins from Drosophila melanogaster. J Bio Chem. 2002;277(15):13229–13236. doi: 10.1074/jbc.M110502200 11821393

35. Hsu PD, Lander ES, Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell. 2014;157(6):1262–1278. doi: 10.1016/j.cell.2014.05.010 24906146

36. Zeng B, Zhan S, Wang Y, Huang YP, Xu J, Liu Q et al. Expansion of CRISPR targeting sites in Bombyx mori. Insect Biochem Mol Biol. 2016;72:31–40. doi: 10.1016/j.ibmb.2016.03.006 27032928

37. Wang SL, Wang WW, Ma Q, Shen ZF, Zhang MQ, Zhou NM et al. Elevenin signaling modulates body color through the tyrosine-mediated cuticle melanism pathway. FASEB J. 2019;33(9):9731–9741. doi: 10.1096/fj.201802786RR 31162939

38. Tobias F, Dominik H, Boris B, Nicola Z. High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Analytical Chemistry. 2011;83(18):7074–7080. doi: 10.1021/ac201267k 21830798

39. Fujii T, Banno Y. Identification of a novel function of the silkworm integument in nitrogen metabolism: Uric acid is synthesized within the epidermal cells in B. mori. Insect Biochem Mol Biol. 2019;105(1):43–50. doi: 10.1016/j.ibmb.2018.12.014 30610924

40. Dembeck LM, Wen H, Magwire MM, Faye L, Lyman RF, Mackay TFC. Genetic architecture of abdominal pigmentation in Drosophila melanogaster. Plos Genetics. 2015;11(5):e1005163. doi: 10.1371/journal.pgen.1005163 25933381

41. Wittkopp PJ, Williams BL, Selegue JE, Carroll SB. Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc Natl Acad Sci USA.2003; 100(4):1808–1813. doi: 10.1073/pnas.0336368100 12574518

42. Jin H, Seki T, Yamaguchi J, Fujiwara H. Prepatterning of Papilio xuthus caterpillar camouflage is controlled by three homeobox genes:clawless, abdominal-A, and Abdominal-B. Science Advances. 2019;5(4):eaav7569. doi: 10.1126/sciadv.aav7569 30989117

43. Wittkopp PJ, True JR, Carroll SB. Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development. 2002;129(8):1849–1858. doi: 10.2193/0022-541X(2005)0692.0.CO;2 11934851

44. Li XT, Shi LG, Dai XP, Chen YJ, Xie HQ, Feng M, et al. Expression plasticity and evolutionary changes extensively shape the sugar-mimic alkaloid adaptation of nondigestive glucosidase in lepidopteran mulberry-specialist insects. Molecular ecology. 2018;27(13):2858–2870. doi: 10.1111/mec.14720 29752760

45. Simmons MP. Relative benefits of amino-acid, codon, degeneracy, DNA, and purine-pyrimidine character coding for phylogenetic analyses of exons. J Syst Evol, 2017; 55(2):85–109. doi: 10.1111/jse.12233

46. Guang Y, David K., Smith H, et al. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution. 2017;8(1): 28–26. doi: 10.1111/2041-210X.12628

47. Pan Y, Lv P, Wang Y, Yin LJ, Ma HX, Ma GH, et al. In silico identification of novel chitinase-like proteins in the silkworm, Bombyx mori. J Insect Sci. 2012;12(1). doi: 10.1673/031.012.15001 23461297

48. Zhang ZJ, Zhang SS, Niu BL, Ji DF, Liu XJ, Li MW, et al. A determining factor for insect feeding preference in the silkworm, Bombyx mori. PLoS Biol. 2019;17(2):e3000162. doi: 10.1371/journal.pbio.3000162 30811402

49. Zhou YY, Li XT, Katsuma S, Xu YS, Shi LG, Shimada T, et al. Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects. Molecular ecology. 2019;28(24):5282–5298. doi: 10.1111/mec.15291 31674075

50. Bao L, Gao H, Zheng Z, Zhao X, Zhang M, Jiao F, et al. Integrated transcriptomic and un-targeted metabolomics analysis reveals Mulberry Fruit (Morus atropurpurea) in response to sclerotiniose pathogen ciboria shiraiana infection. J. Mol. Sci. 2020; 21, 1789. doi: 10.3390/ijms21051789 32150966


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