The beta-1, 4-N-acetylglucosaminidase 1 gene, selected by domestication and breeding, is involved in cocoon construction of Bombyx mori

English version

Autoři: Chunlin Li ^aff001; Xiaoling Tong ^aff001; Weidong Zuo ^aff001; Hai Hu ^aff001; Gao Xiong ^aff001; Minjin Han ^aff001; Rui Gao ^aff001; Yue Luan ^aff001; Kunpeng Lu ^aff001; Tingting Gai ^aff001; Zhonghuai Xiang ^aff001; Cheng Lu ^aff001; Fangyin Dai ^aff001
Působiště autorů: State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, Chongqing, China ^aff001
Vyšlo v časopise: The beta-1, 4-N-acetylglucosaminidase 1 gene, selected by domestication and breeding, is involved in cocoon construction of Bombyx mori. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008907
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008907

Souhrn

Holometabolous insects have distinct larval, pupal, and adult stages. The pupal stage is typically immobile and can be subject to predation, but cocoon offers pupal protection for many insect species. The cocoon provides a space in which the pupa to adult metamorphosis occurs. It also protects the pupa from weather, predators and parasitoids. Silk protein is a precursor of the silk used in cocoon construction. We used the silkworm as a model species to identify genes affecting silk protein synthesis and cocoon construction. We used quantitative genetic analysis to demonstrate that β-1,4-N-acetylglucosaminidase 1 (BmGlcNase1) is associated with synthesis of sericin, the main composite of cocoon. BmGlcNase1 has an expression pattern coupled with silk gland development and cocoon shell weight (CSW) variation, and CSW is an index of the ability to synthesize silk protein. Up-regulated expression of BmGlcNase1 increased sericin content by 13.9% and 22.5% while down-regulation reduced sericin content by 41.2% and 27.3% in the cocoons of females and males, respectively. Genomic sequencing revealed that sequence variation upstream of the BmGlcNase1 transcriptional start site (TSS) is associated with the expression of BmGlcNase1 and CSW. Selective pressure analysis showed that GlcNase1 was differentially selected in insects with and without cocoons (ω₁ = 0.044 vs. ω₂ = 0.154). This indicates that this gene has a conserved function in the cocooning process of insects. BmGlcNase1 appears to be involved in sericin synthesis and silkworm cocooning.

Klíčová slova:

Domestic animals – Evolutionary genetics – Genotyping – Insects – Larvae – Protein synthesis – Silkworms – Silk

Zdroje

1. Sutherland TD, Young JH, Weisman S, Hayashi CY, Merritt DJ. Insect silk: one name, many materials. Annu Rev Entomol. 2010; 55: 171–88. doi: 10.1146/annurev-ento-112408-085401 19728833

2. Xiang ZH. Quantitative trait genetics of silkworm. In: Xiang ZH, editor. Biology of Sericulture. Forestry Press of China, Beijing; 2005. pp. 242–53.

3. Andersson M, Johansson J, Rising A. Silk Spinning in Silkworms and Spiders. Int J Mol Sci. 2016; 17: 1290.

4. Sparkes J, Holland C. Analysis of the pressure requirements for silk spinning reveals a pultrusion dominated process. Nat Commun. 2017; 8: 594. doi: 10.1038/s41467-017-00409-7 28928362

5. Gong Y, Li L, Gong D, Yin H, Zhang J. Biomolecular Evidence of Silk from 8,500 Years Ago. PLoS One. 2016; 11(12):e0168042. doi: 10.1371/journal.pone.0168042 27941996

6. Yang SY, Han MJ, Kang LF, Li ZW, Shen YH, Zhang Z. Demographic history and gene flow during silkworm domestication. BMC Evol Biol. 2014; 14: 185. doi: 10.1186/s12862-014-0185-0 25123546

7. Lu C, Li B, Zhao AC, Xiang ZH. QTL mapping of economically important traits in Silkworm (Bombyx mori). Science in China Ser. C Life Sciences. 2004; 47: 477–484. doi: 10.1360/03yc0260 15623161

8. Mirhoseini SZ, Rabiei B, Potki P, Dalirsefat SB. Amplified fragment length polymorphism mapping of quantitative trait loci for economically important traits in the silkworm, Bombyx mori. J Insect Sci. 2010; 10: 153. doi: 10.1673/031.010.14113 21070171

9. Lie Z, Cheng L, Dai FY, Fang SM. Mapping of major quantitative trait loci for economic traits of silkworm cocoon. Genet Mol Res. 2010; 9: 78–88. doi: 10.4238/vol9-1gmr676 20092037

10. Zhan S, Huang J, Guo Q, Zhao Y, Li W, Miao X, et al. An integrated genetic linkage map for silkworms with three parental combinations and its application to the mapping of single genes and QTL. BMC Genomics. 2009; 10: 389. doi: 10.1186/1471-2164-10-389 19698097

11. Li C, Zuo WD, Tong XL, Hu H, Qiao L, Song JB, et al. A composite method for mapping quantitative trait loci without interference of female achiasmatic and gender effects in silkworm, Bombyx mori. Anim Genet. 2015; 46: 426–32. doi: 10.1111/age.12311 26059330

12. Xia Q, Guo Y, Zhang Z, Li D, Xuan Z, Li Z, et al. Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx mori). Science. 2009; 326: 433–6. doi: 10.1126/science.1176620 19713493

13. Xiang H. Liu X, Li M, Zhu Y, Wang L, Cui Y, et al. The evolutionary road from wild moth to domestic silkworm. Nat Ecol Evol. 2018; 2: 1268–1279. doi: 10.1038/s41559-018-0593-4 29967484

14. Li C, Tong XL, Zuo WD, Luan Y, Gao R, Han MJ, et al. QTL analysis of cocoon shell weight identifies BmRPL18 associated with silk protein synthesis in silkworm by pooling sequencing. Sci Rep. 2017; 7: 17985. doi: 10.1038/s41598-017-18277-y 29269837

15. Darvasi A, Soller M. Selective genotyping for determination of linkage between a marker locus and a quantitative trait locus. Theor Appl Genet. 1992; 85: 353–359. doi: 10.1007/BF00222881 24197326

16. Fang SM, Hu BL, Zhou QZ, Yu QY, Zhang Z. Comparative analysis of the silk gland transcriptomes between the domestic and wild silkworms. BMC Genomics. 2015; 16:60. doi: 10.1186/s12864-015-1287-9 25887670

17. Dong Y, Dai FY, Ren YD, Liu H, Chen L, Yang PC, et al. Comparative transcriptome analyses on silk glands of six silkmoths imply the genetic basis of silk structure and coloration. BMC Genomics. 2015; 16:203. doi: 10.1186/s12864-015-1420-9 25886738

18. Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer. 2015; 15: 540–55. doi: 10.1038/nrc3982 26289314

19. Love DC, Hanover JA. The hexosamine signaling pathway: deciphering the "O-GlcNAc code". Sci STKE. 2005; 312: re13.

20. Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology. 1993; 3: 97–130. doi: 10.1093/glycob/3.2.97 8490246

21. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, et al. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell. 2007; 129: 123–34. doi: 10.1016/j.cell.2007.01.049 17418791

22. Huang B, Wu Q, Ge Y, Zhang J, Sun L, Zhang Y, et al. Expression of N-acetylglucosaminyltransferase V in gastric cancer correlates with metastasis and prognosis. Int J Oncol. 2014; 44: 849–57. doi: 10.3892/ijo.2014.2248 24399258

23. Takahashi N, Yamamoto E, Ino K, Miyoshi E, Nagasaka T, Kajiyama H, et al. High expression of N-acetylglucosaminyltransferase V in mucinous tumors of the ovary. Oncol Rep. 2009; 22: 1027–32. doi: 10.3892/or_00000531 19787216

24. Lau KS, Dennis JW. N-Glycans in cancer progression. Glycobiology. 2008; 18: 750–60. doi: 10.1093/glycob/cwn071 18701722

25. Zhou SB, Dong W, Zhao LJ. Discussion on Incorporating Sericin Content into Cocoon Quality Assessment System. Management and Depth. 2008; 11: 34–36.

26. Xiang ZH. Quantitative trait genetics of silkworm. In: Xiang ZH, editor. Biology of Sericulture. Forestry Press of China, Beijing; 2005. pp. 305–06.

27. Liu T, Zhang H, Liu F, Wu Q, Shen X, Yang Q. Structural determinants of an insect beta-N-Acetyl-D-hexosaminidase specialized as a chitinolytic enzyme. J Biol Chem. 2011; 286: 4049–58. doi: 10.1074/jbc.M110.184796 21106526

28. Hogenkamp DG, Arakane Y, Kramer KJ, Muthukrishnan S, Beeman RW. Characterization and expression of the beta-N-acetylhexosaminidase gene family of Tribolium castaneum. Insect Biochem Mol Biol. 2008; 38: 478–89. doi: 10.1016/j.ibmb.2007.08.002 18342252

29. Stern DL. The genetic causes of convergent evolution. Nat Rev Genet. 2013; 14: 751–64. doi: 10.1038/nrg3483 24105273

30. Dobler S, Dalla S, Wagschal V, Agrawal A. A. Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase. Proc Natl Acad Sci U S A. 2012; 109: 13040–5. doi: 10.1073/pnas.1202111109 22826239

31. Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P. Parallel molecular evolution in an herbivore community. Science. 2012; 337: 1634–7. doi: 10.1126/science.1226630 23019645

32. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal GJ, Dickson M, Grimwood J, et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science. 2005; 307: 1928–33. doi: 10.1126/science.1107239 15790847

33. Olofsson JK. Bianconi M, Besnard, Dunning LT, Lundgren MR, Holota H, et al. Genome biogeography reveals the intraspecific spread of adaptive mutations for a complex trait. Mol Ecol. 2016; 25: 6107–6123. doi: 10.1111/mec.13914 27862505

34. Song Y. Endepols S, Klemann N, Richter D, Matuschka FR, Shih CH, et al. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between old world mice. Curr Biol. 2011; 21: 1296–301. doi: 10.1016/j.cub.2011.06.043 21782438

35. Nagaraja GM, Nagaraju J. Genome fingerprinting of the silkworm, Bombyx mori, using random arbitrary primers. Electrophoresis. 1995;16(9):1633–8. doi: 10.1002/elps.11501601270 8582347

36. Wang F, Xu H, Yuan L, Ma S, Wang Y, Duan X, et al. An optimized sericin-1 expression system for mass-producing recombinant proteins in the middle silk glands of transgenic silkworms. Transgenic Res. 2013; 22: 925–38. doi: 10.1007/s11248-013-9695-6 23435751

37. Zhao AC, Zhao TF, Zhang YS, Xia QY, Lu C, Zhou ZY, et al. New and highly efficient expression systems for expressing selectively foreign protein in the silk glands of transgenic silkworm. Transgenic Res, 2010; 19: 29–44. doi: 10.1007/s11248-009-9295-7 19533404

38. Dai ZJ, Sun W, Zhang Z. Comparative analysis of iTRAQ-based proteomes for cocoons between the domestic silkworm (Bombyx mori) and wild silkworm (Bombyx mandarina). J Proteomics. 2019; 192: 366–373. doi: 10.1016/j.jprot.2018.09.017 30287406

39. Axelsson E, Ratnakumar A, Arendt ML, Maqbool K, Webster MT, Perloski M, et al. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature. 2013; 495(7441): 360–4. doi: 10.1038/nature11837 23354050

40. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Datasets. Mol. Biol. Evol. 2017; 34: 3299–3302. doi: 10.1093/molbev/msx248 29029172

41. Gao F, Chen C, Arab DA, Du Z, He Y, Ho SYW. EasyCodeML: A visual tool for analysis of selection using CodeML. Ecology and Evolution. 2019; 9(7):3891–3898. doi: 10.1002/ece3.5015 31015974

42. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016; 33(7):1870–4. doi: 10.1093/molbev/msw054 27004904

Článek A non-canonical RNAi pathway controls virulence and genome stability in Mucorales

Článek TaTLP1 interacts with TaPR1 to contribute to wheat defense responses to leaf rust fungus

Článek Linking protein to phenotype with Mendelian Randomization detects 38 proteins with causal roles in human diseases and traits

Článek Epistatic interactions between PHOTOPERIOD1, CONSTANS1 and CONSTANS2 modulate the photoperiodic response in wheat

Článek Conditional knockout of RAD51-related genes in Leishmania major reveals a critical role for homologous recombination during genome replication

Článek Predicting longevity responses to dietary restriction: A stepping stone toward precision geroscience

Článek Genetic and metabolomic architecture of variation in diet restriction-mediated lifespan extension in Drosophila

Článek Repression of tick microRNA-133 induces organic anion transporting polypeptide expression critical for Anaplasma phagocytophilum survival in the vector and transmission to the vertebrate host

Článek Brassinosteroids regulate root meristem development by mediating BIN2-UPB1 module in Arabidopsis

Článek The membrane protein ANKH is crucial for bone mechanical performance by mediating cellular export of citrate and ATP

Článek A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata

Článek A Drosophila model of Pontocerebellar Hypoplasia reveals a critical role for the RNA exosome in neurons