Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Horizontally acquired cysteine synthase genes undergo functional divergence in lepidopteran herbivores

Abstract

Horizontal gene transfer (HGT) plays an important role in evolutionary processes as organisms adapt to their environments, and now cases of gene duplication after HGT in eukaryotes are emerging at an increasing rate. However, the fate and roles of the duplicated genes over time in eukaryotes remain unclear. Here we conducted a comprehensive analysis of the evolution of cysteine synthase (CYS) in lepidopteran insects. Our results indicate that HGT-derived CYS genes are widespread and have undergone duplication following horizontal transfer in many lepidopteran insects. Moreover, lepidopteran CYS proteins not only have β-cyanoalanine synthase activity but also possess cysteine synthase activity that is involved in sulfur amino acid biosynthesis. Duplicated CYS genes show marked divergence in gene expression patterns and enzymatic properties, suggesting that they probably have undergone subfunctionalization and/or neofunctionalization in Lepidoptera. The gene transfer of CYS genes and subsequent duplication appears to have facilitated the adaptation of lepidopteran insects to different diets and promoted their ecological diversification. Overall, this study provides valuable insights into the ecological and evolutionary contributions of CYS in lepidopteran insects.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Phylogenetic analysis of CYSs.
Fig. 2: Identification of CYS copy number in mites and Lepidoptera.
Fig. 3: Synteny of genes flanking CYS in mite and 11 lepidopteran chromosomes.
Fig. 4: Expression profiles of CYS in Bombyx mori.
Fig. 5: Expression profiles of CYS in Spodoptera frugiperda.
Fig. 6: The CAS activity analysis of BmorCYS/SfruCYS1/SfruCYS2.
Fig. 7: The CYS activity analysis of BmorCYS/SfruCYS1/SfruCYS2.
Fig. 8: Summary of the synthesis and metabolism of cysteine in lepidopteran larvae.

Data availability

qRT-PCR data is available from the Dryad Digital Repository https://doi.org/10.5061/dryad.pzgmsbckj.

References

  1. Acuna R, Padilla BE, Florez-Ramos CP, Rubio JD, Herrera JC, Benavides P et al. (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci USA 109(11):4197–4202

    CAS  PubMed  Article  Google Scholar 

  2. Aoyama K, Watabe M, Nakaki T (2008) Regulation of neuronal glutathione synthesis. J Pharm Sci 108(3):227–238

    CAS  Article  Google Scholar 

  3. Arias M, Meichanetzoglou A, Elias M, Rosser N, de-Silva DL, Nay B et al. (2016) Variation in cyanogenic compounds concentration within a Heliconius butterfly community: does mimicry explain everything? BMC Evol Biol 16(1):272

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  4. Baloch MN, Fan JY, Haseeb M, Zhang RZ (2020) Mapping potential distribution of Spodoptera frugiperda (Lepidoptera: Noctuidae) in central Asia. Insects 11(3):172

    PubMed Central  Article  PubMed  Google Scholar 

  5. Barbehenn RV, Kochmanski J, Menachem B, Poirier LM (2013a) Allocation of cysteine for glutathione production in caterpillars with different antioxidant defense strategies: a comparison of Lymantria dispar and Malacosoma disstria. Arch Insect Biochem 84(2):90–103

    CAS  Google Scholar 

  6. Barbehenn RV, Niewiadomski J, Kochmanski J (2013b) Importance of protein quality versus quantity in alternative host plants for a leaf-feeding insect. Oecologia 173(1):1–12

    PubMed  Article  Google Scholar 

  7. Bogicevic B, Berthoud H, Portmann R, Meile L, Irmler S (2012) CysK from Lactobacillus casei encodes a protein with O-acetylserine sulfhydrylase and cysteine desulfurization activity. Appl Microbiol Biot 94(5):1209–1220

    CAS  Article  Google Scholar 

  8. Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280(46):38803–38813

    CAS  PubMed  Article  Google Scholar 

  9. Boto L (2014) Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc Biol Sci 281(1777):20131834

    Google Scholar 

  10. Brown ES, Dewhurst CF (2009) The genus Spodoptera (Lepidoptera, Noctuidae) in Africa and the Near East. Bull Entomological Res 65(2):221–262

    Article  Google Scholar 

  11. Budde MW, Roth MB (2011) The response of Caenorhabditis elegans to hydrogen sulfide and hydrogen cyanide. Genetics 189(2):521–532

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. Burkhard P, Rao GS, Hohenester E, Schnackerz KD, Cook PF, Jansonius JN (1998) Three-dimensional structure of O-acetylserine sulfhydrylase from Salmonella typhimurium. J Mol Biol 283(1):121–133

    CAS  PubMed  Article  Google Scholar 

  13. Dai X, Li R, Li X, Liang Y, Gao Y, Xu Y et al. (2019) Gene duplication and subsequent functional diversification of sucrose hydrolase in Papilio xuthus. Insect Mol Biol 28(6):862–872

    CAS  PubMed  Article  Google Scholar 

  14. Daimon T, Katsuma S, Iwanaga M, Kang WK, Shimada T (2005) The BmChi-h gene, a bacterial-type chitinase gene of Bombyx mori, encodes a functional exochitinase that plays a role in the chitin degradation during the molting process. Insect Biochem Mol Biol 35(10):1112–1123

    CAS  PubMed  Article  Google Scholar 

  15. Daimon T, Taguchi T, Meng Y, Katsuma S, Mita K, Shimada T (2008) Beta-fructofuranosidase genes of the silkworm, Bombyx mori - Insights into enzymatic adaptation of B. mori to toxic alkaloids in mulberry latex. J Biol Chem 283(22):15271–15279

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Danchin EG, Rosso MN, Vieira P, de Almeida-Engler J, Coutinho PM, Henrissat B et al. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107(41):17651–17656

    CAS  PubMed  Article  Google Scholar 

  17. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27(8):1164–1165

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. Doxey AC, Yaish MWF, Moffatt BA, Griffith M, McConkey BJ (2007) Functional divergence in the Arabidopsis beta-1,3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 24(4):1045–1055

    CAS  PubMed  Article  Google Scholar 

  19. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7(10):e1002195

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. Bmc Bioinforma 5:1–19

    Article  CAS  Google Scholar 

  21. Fan X, Qiu H, Han W, Wang Y, Xu D, Zhang X et al. (2020) Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions. Sci Adv 6(18):eaba0111

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Farre D, Alba MM (2010) Heterogeneous patterns of gene-expression diversification in mammalian gene duplicates. Mol Biol Evol 27(2):325–335

    CAS  PubMed  Article  Google Scholar 

  23. Feldman-Salit A, Wirtz M, Hell R, Wade RC (2009) A mechanistic model of the cysteine synthase complex. J Mol Biol 386(1):37–59

    CAS  PubMed  Article  Google Scholar 

  24. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Gaitonde MK (1967) A spectrophotometric method for direct determination of cysteine in presence of other naturally occurring amino acids. Biochem J 104(2):627–633

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Gan Q, Zhang XW, Zhang DB, Shi L, Zhou Y, Sun TT et al. (2018) BmSUC1 is essential for glycometabolism modulation in the silkworm, Bombyx mori. BBA-Gene Regul Mech 1861(6):543–553

    CAS  Google Scholar 

  27. Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24(10):2298–2309

    CAS  PubMed  Article  Google Scholar 

  28. Gao Y, Liu YC, Jia SZ, Liang YT, Tang Y, Xu YS et al. (2020) Imaginal disc growth factor maintains cuticle structure and controls melanization in the spot pattern formation of Bombyx mori. PLoS Genet 16(9):e1008980

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Goldsmith MR, Shimada T, Abe H (2005) The genetics and genomics of the silkworm, Bombyx mori. Annu Rev Entomol 50:71–100

    CAS  PubMed  Article  Google Scholar 

  30. Gu X, Zhang ZQ, Huang W (2005) Rapid evolution of expression and regulatory divergences after yeast gene duplication. Proc Natl Acad Sci USA 102(3):707–712

    CAS  PubMed  Article  Google Scholar 

  31. Gu ZL, Nicolae D, Lu HHS, Li WH (2002) Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet 18(12):609–613

    CAS  PubMed  Article  Google Scholar 

  32. Helmkampf M, Cash E, Gadau J (2015) Evolution of the insect desaturase gene family with an emphasis on social Hymenoptera. Mol Biol Evol 32(2):456–471

    PubMed  Article  Google Scholar 

  33. Hendrickson HR, Conn EE (1969) Cyanide metabolism in higher plants. IV. Purification and properties of the beta-cyanolanine synthase of blue lupine. J Biol Chem 244(10):2632–2640

    CAS  PubMed  Article  Google Scholar 

  34. Herfurth AM, van Ohlen M, Wittstock U (2017) Beta-cyanoalanine synthases and their possible role in Pierid host plant adaptation. Insects 8(2):62

    PubMed Central  Article  PubMed  Google Scholar 

  35. Husnik F, McCutcheon JP (2018) Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol 16(2):67–79

    CAS  PubMed  Article  Google Scholar 

  36. Jeschke V, Gershenzon J, Vassao DG (2016) A mode of action of glucosinolate-derived isothiocyanates: detoxification depletes glutathione and cysteine levels with ramifications on protein metabolism in Spodoptera littoralis. Insect Biochem Molec 71:37–48

    CAS  Article  Google Scholar 

  37. Jiggins FM, Hurst GD (2011) Microbiology. Rapid insect evolution by symbiont transfer. Science 332(6026):185–186

    CAS  PubMed  Article  Google Scholar 

  38. Koonin EV, Makarova KS, Aravind L (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    CAS  Article  Google Scholar 

  40. Lai KW, Yau CP, Tse YC, Jiang LW, Yip WK (2009) Heterologous expression analyses of rice OsCAS in Arabidopsis and in yeast provide evidence for its roles in cyanide detoxification rather than in cysteine synthesis in vivo. J Exp Bot 60(3):993–1008

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Lee BS, Huang JS, Jayathilaka LP, Lee J, Gupta S (2016) Antibody production with synthetic peptides. Methods Mol Biol 1474:25–47

    CAS  PubMed  Article  Google Scholar 

  42. Lee HL, Irish VF (2011) Gene duplication and loss in a MADS box gene transcription factor circuit. Mol Biol Evol 28(12):3367–3380

    CAS  PubMed  Article  Google Scholar 

  43. Leite DJ, Baudouin-Gonzalez L, Iwasaki-Yokozawa S, Lozano-Fernandez J, Turetzek N, Akiyama-Oda Y et al. (2018) Homeobox gene duplication and divergence in arachnids. Mol Biol Evol 35(9):2240–2253

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. Li ZW, Shen YH, Xiang ZH, Zhang Z (2011) Pathogen-origin horizontally transferred genes contribute to the evolution of lepidopteran insects. Bmc Evolut Biol 11(1):356

    CAS  Article  Google Scholar 

  45. Liu HJ, Tang ZX, Han XM, Yang ZL, Zhang FM, Yang HL et al. (2015) Divergence in enzymatic activities in the soybean GST supergene family provides new insight into the evolutionary dynamics of whole-genome duplicates. Mol Biol Evol 32(11):2844–2859

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Lunn JE, Droux M, Martin J, Douce R (1990) Localization of atp sulfurylase and O-acetylserine(Thiol)lyase in spinach leaves. Plant Physiol 94(3):1345–1352

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154(1):459–473

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Nikoh N, McCutcheon JP, Kudo T, Miyagishima S, Moran NA, Nakabachi A (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. Plos Genet 6(2):e1000827

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  49. Novakova E, Moran NA (2012) Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Mol Biol Evol 29(1):313–323

    CAS  PubMed  Article  Google Scholar 

  50. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304

    CAS  PubMed  Article  Google Scholar 

  51. Pallen MJ, Wren BW (2007) Bacterial pathogenomics. Nature 449(7164):835–842

    CAS  PubMed  Article  Google Scholar 

  52. Polz MF, Alm EJ, Hanage WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29(3):170–175

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. Rane RV, Walsh TK, Pearce SL, Jermiin LS, Gordon KH, Richards S et al. (2016) Are feeding preferences and insecticide resistance associated with the size of detoxifying enzyme families in insect herbivores? Curr Opin Insect Sci 13:70–76

    PubMed  Article  Google Scholar 

  54. Schramm K, Vassao DG, Reichelt M, Gershenzon J, Wittstock U (2012) Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem Molec 42(3):174–182

    CAS  Article  Google Scholar 

  55. Stauber EJ, Kuczka P, van Ohlen M, Vogt B, Janowitz T, Piotrowski M et al. (2012) Turning the ‘mustard oil bomb’ into a ‘cyanide bomb’: aromatic glucosinolate metabolism in a specialist insect herbivore. Plos One 7(4):e35545

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. Sun BF, Xiao JH, He SM, Liu L, Murphy RW, Huang DW (2013) Multiple ancient horizontal gene transfers and duplications in lepidopteran species. Insect Mol Biol 22(1):72–87

    CAS  PubMed  Article  Google Scholar 

  57. Suzuki K, Moriguchi K, Yamamoto S (2015) Horizontal DNA transfer from bacteria to eukaryotes and a lesson from experimental transfers. Res Microbiol 166(10):753–763

    CAS  PubMed  Article  Google Scholar 

  58. Van Ohlen M, Herfurth AM, Kerbstadt H, Wittstock U (2016) Cyanide detoxification in an insect herbivore: molecular identification of beta-cyanoalanine synthases from Pieris rapae. Insect Biochem Molec 70:99–110

    CAS  Article  Google Scholar 

  59. Wada M, Awano N, Yamazawa H, Takagi H, Nakamori S (2004) Purification and characterization of O-acetylserine sulfhydrylase of Corynebacterium glutamicum. Biosci Biotech Bioch 68(7):1581–1583

    CAS  Article  Google Scholar 

  60. Wadleigh RW, Yu SJ (1988) Detoxification of isothiocyanate allelochemicals by glutathione transferase in three lepidopterous species. J Chem Ecol 14(4):1279–1288

    CAS  PubMed  Article  Google Scholar 

  61. Wagner A (2002) Asymmetric functional divergence of duplicate genes in yeast. Mol Biol Evol 19(10):1760–1768

    CAS  PubMed  Article  Google Scholar 

  62. Wybouw N, Dermauw W, Tirry L, Stevens C, Grbic M, Feyereisen R et al. (2014) A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. Elife 3:e02365

    PubMed  PubMed Central  Article  Google Scholar 

  63. Wybouw N, Pauchet Y, Heckel DG, Van Leeuwen T (2016) Horizontal gene transfer contributes to the evolution of arthropod herbivory. Genome Biol Evol 8(6):1785–1801

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. Yamaguchi Y, Nakamura T, Kusano T, Sano H (2000) Three arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase. Plant Cell Physiol 41(4):465–476

    CAS  PubMed  Article  Google Scholar 

  65. Yi H, Juergens M, Jez JM (2012) Structure of soybean beta-cyanoalanine synthase and the molecular basis for cyanide detoxification in plants. Plant Cell 24(6):2696–2706

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. Zhou YY, Li XT, Katsuma S, Xu YS, Shi LG, Shimada T et al. (2019) Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects. Mol Ecol 28(24):5282–5298

    CAS  PubMed  Article  Google Scholar 

  67. Zhu B, Lou MM, Xie GL, Zhang GQ, Zhou XP, Li B et al. (2011) Horizontal gene transfer in silkworm, Bombyx mori. Bmc Genomics 12:248

    PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgements

We thank Professor Jianhong Xu for helpful comments on this study. We are indebted to Professor Yuxian He, Professor Wenwu Zhou, Shunze Jia, and Qiong Wu for technical support. This work was supported by the National Natural Science Foundation of China (Grant nos. 31970460, 31602010, and 31572321).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Huabing Wang.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor Ben Evans

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Zhou, Y., Jing, W. et al. Horizontally acquired cysteine synthase genes undergo functional divergence in lepidopteran herbivores. Heredity (2021). https://doi.org/10.1038/s41437-021-00430-z

Download citation

Search

Quick links