Transcriptomic analysis of the bagworm moth silk gland reveals a number of silk genes conserved within Lepidoptera.
Eumeta variegata
bagworm moth
fibroin
gene expression
silk gland
transcriptomic analysis
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
revised:
25
05
2020
received:
17
03
2020
accepted:
19
06
2020
pubmed:
27
6
2020
medline:
10
8
2021
entrez:
27
6
2020
Statut:
ppublish
Résumé
Lepidopteran insects produce cocoons with unique properties. The cocoons are made of silk produced in the larval tissue silk gland and our understanding of the silk genes is still very limited. Here, we investigated silk genes in the bagworm moth Eumeta variegata, a species that has recently been found to produce extraordinarily strong and tough silk. Using short-read transcriptomic analysis, we identified a partial sequence of the fibroin heavy chain gene and its product was found to have a C-terminal structure that is conserved within nonsaturniid species. This is in accordance with the presence of fibroin light chain/fibrohexamerin genes and it is suggested that the bagworm moth is producing silk composed of fibroin ternary complex. This indicates that the fibroin structure has been evolutionarily conserved longer than previously thought. Other than fibroins we identified candidates for sericin genes, expressed strongly in the middle region of the silk gland and encoding serine-rich proteins, and other silk genes, that are structurally conserved with other lepidopteran homologues. The bagworm moth is thus considered to be producing conventional lepidopteran type of silk. We further found a number of genes expressed in a specific region of the silk gland and some genes showed conserved expression with Bombyx mori counterparts. This is the first study allowing comprehensive silk gene identification and expression analysis in the lepidopteran Psychidae family and should contribute to the understanding of silk gene evolution as well as to the development of novel types of silk.
Identifiants
pubmed: 32589338
doi: 10.1111/1744-7917.12846
doi:
Substances chimiques
Insect Proteins
0
L-chain, fibroin protein, insect
0
Sericins
0
Silk
0
fhx protein, Bombyx mori
0
Fibroins
9007-76-5
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
885-900Subventions
Organisme : SATREPS (Science and Technology Research Partnership for Sustainable Development)
Informations de copyright
© 2020 Institute of Zoology, Chinese Academy of Sciences.
Références
Akai, H. (1976) The silk gland. Ultrastructural Morphology of Insects (ed. H. Akai), pp. 57-114. University of Tokyo Press, Tokyo.
Bello, B., Horard, B. and Couble, P. (1994) The selective expression of silk-protein encoding genes in Bombyx mori silk gland. Bulletin de I'lnstitut Pasteur, 92, 81-100.
Bolger, A. M., Lohse, M. and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.
Chang, H., Cheng, T., Wu, Y., Hu, W., Long, R., Liu, C. et al. (2015) Transcriptomic analysis of the anterior silk gland in the domestic silkworm (Bombyx mori)-insight into the mechanism of silk formation and spinning. PLoS ONE, 10, e0139424.
Cheng, T., Fu, B., Wu, Y., Long, R., Liu, C. and Xia, Q. (2015) Transcriptome sequencing and positive selected genes analysis of Bombyx mandarina. PLoS ONE, 10, e0122837.
Chetia, H., Kabiraj, D., Singh, D., Mosahari, P.V., Das, S., Sharma, P. et al. (2017) De novo transcriptome of the muga silkworm, Antheraea assamensis (Helfer). Gene, 611, 54-65.
Collin, M.A., Mita, K., Sehnal, F. and Hayashi, C.Y. (2010) Molecular evolution of lepidopteran silk proteins: insights from the ghost moth, Hepialus californicus. Journal of Molecular Evolution, 70, 519-529.
Dong, Y., Dai, F., Ren, Y., Liu, H., Chen, L., Yang, P. et al. (2015) Comparative transcriptome analysis on silk glands of six silkmoths imply the genetic basis of silk structure and coloration. BMC Genomics, 16, 203.
Dong, Z., Guo, K., Zhang, X., Zhang, T., Zhang, Y., Ma, S. et al. (2019) Identification of Bombyx mori sericin 4 protein as a new biological adhesive. International Journal of Biological Macromolecules, 132, 1121-1130.
Fang, S.M., Hu, B.L., Zhou, Q.Z., Yu, Q.Y. and Zhang, Z. (2015) Comparative analysis of the silk gland transcriptomes between the domestic and wild silkworms. BMC Genomics, 16, 60.
Fedič, R., Žurovec, M. and Sehnal, F. (2003) Correlation between fibroin amino acid sequence and physical silk properties. The Journal of Biological Chemistry, 278, 35255-35264.
Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.W., Amit, I. et al. (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-seq data. Nature Biotechnology, 29, 644-652.
Gupta, A.K., Mita, K., Arunkumar, K.P. and Nagaraju, J. (2015) Molecular architecture of silk fibroin of Indian golden silkmoth, Antheraea assama. Scientific Reports, 5, 12706.
Hwang, J.S., Lee, J.S., Goo, T.W., Yun, E.Y., Lee, K.S., Kim, Y.S. et al. (2001) Cloning of the fibroin gene from the oak silkworm, Antheraea yamamai and its complete sequence. Biotechnology Letters, 23, 1321-1326.
Inoue, S., Tanaka, K., Arisaka, F., Kimura, S., Ohtomo, K. and Mizuno, S. (2000) Silk fibroin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and P25, with a 6:6:1 molar ratio. The Journal of Biological Chemistry, 275, 40517-40528.
Jouraku, A., Yamamoto, K., Kuwazaki, S., Urio, M., Suetsugu, Y., Narukawa, J. et al. (2013) KONAGAbase: a genomic and transcriptomic database for the diamondback moth, Plutella xylostella. BMC Genomics, 14, 464.
Kim, J.S., Kim, M.J., Jeong, J.S. and Kim, I. (2018) Complete mitochondrial genome of Saturnia jonasii (Lepidoptera: Saturniidae): genomic comparisons and phylogenetic inference among Bombycoidea. Genomics, 110, 274-282.
Kimoto, M., Tsubota, T., Uchino, K., Sezutsu, H. and Takiya, S. (2014) Hox transcription factor Antp regulates sericin-1 gene expression in the terminal differentiated silk gland of Bombyx mori. Developmental Biology, 386, 64-71.
Kimoto, M., Tsubota, T., Uchino, K., Sezutsu, H. and Takiya, S. (2015) LIM-homeodomain transcription factor Awh is a key component activating all three fibroin genes, fibH, fibL and fhx, in the silk gland of the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology, 56, 29-35.
Kono, N., Nakamura, H., Ohtoshi, R., Tomita, M., Numata, K. and Arakawa, K. (2019) The bagworm genome reveals a unique fibroin gene that provides high tensile strength. Communications Biology, 2, 148.
Kucerova, L., Zurovec, M., Kludkiewicz, B., Hradilova, M., Strnad, H. and Sehnal, F. (2019) Modular structure, sequence diversification and appropriate nomenclature of seroins produced in the silk glands of Lepidoptera. Scientific Reports, 9, 3797.
Kumar, S., Stecher, G. and Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870-1874.
Kusuda, J., Tazima, Y., Onimaru, K., Ninaki, O. and Suzuki, Y. (1986) The sequence around the 5’ end of the fibroin gene from the wild silkworm, Bombyx mandarina, and comparison with that of the domesticated species, B. mori. Molecular and General Genetics, 203, 359-364.
Langmead, B. and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357-359.
Laskowski, M. and Kato, I. (1980) Protein inhibitors of proteinases. Annual Review of Biochemistry, 49, 593-626.
Leal-Egaña, A. and Scheibel, T. (2010) Silk-based materials for biomedical applications. Biotechnology and Applied Biochemistry, 55, 155-167.
Mitter, C., Davis, D.R. and Cummings, M.P. (2017) Phylogeny and evolution of Lepidoptera. Annual Review of Entomology, 62, 265-283.
Nirmala, X., Mita, K., Vanisree, V., Žurovec, M. and Sehnal, F. (2001) Identification of four small molecular mass proteins in the silk of Bombyx mori. Insect Molecular Biology, 10, 437-445.
Ohno, K., Sawada, J., Takiya, S., Kimoto, M., Matsumoto, A., Tsubota, T. et al. (2013) Silk gland factor-2, involved in fibroin gene transcription, consists of LIM homeodomain, LIM-interacting, and single-stranded DNA-binding proteins. The Journal of Biological Chemistry, 288, 31581-31591.
Okamoto, H., Ishikawa, E. and Suzuki, T. (1982) Structural analysis of sericin genes. The Journal of Biological Chemistry, 257, 15192-15199.
Roberts, A. and Pachter, L. (2013) Streaming fragment assignment for real-time analysis of sequencing experiments. Nature Methods, 10, 71-73.
Royer, C., Briolay, J., Garel, A., Brouilly, P., Sasanuma, S., Sasanuma, M. et al. (2011) Novel genes differentially expressed between posterior and median silk gland identified by SAGE-aided transcriptome analysis. Insect Biochemistry and Molecular Biology, 41, 118-124.
Sezutsu, H., Uchino, K., Kobayashi, I., Tamura, T. and Yukuhiro, K. (2010) Extensive sequence rearrangements and length polymorphism in fibroin genes in the wild silkmoth, Antheraea yamamai (Lepidoptera, Saturniidae). International Journal of Wild Silkmoth & Silk, 15, 35-50.
Sezutsu, H. and Yukuhiro, K. (2000) Dynamic rearrangement within the Antheraea pernyi silk fibroin gene is associated with four types of repetitive units. Journal of Molecular Evolution, 51, 329-338.
Sezutsu, H. and Yukuhiro, K. (2014) The complete nucleotide sequence of the Eri-silkworm (Samia cynthia ricini) fibroin gene. Journal of Insect Biotechnology and Sericology, 83, 59-70.
Su, H., Cheng, Y., Wang, Z., Li, Z., Stanley, D. and Yang, Y. (2015) Silk gland gene expression during larval-pupal transition in the cotton leaf roller Sylepta derogata (Lepidoptera: Pyralidae). PLoS ONE, 10, e0136868.
Sutherland, T.D., Young, J.H., Weisman, S., Hayashi, C.Y. and Merritt, D.J. (2010) Insect silk: one name, many materials. Annual Review of Entomology, 55, 171-188.
Takasu, Y., Hata, T., Uchino, K. and Zhang, Q. (2010) Identification of Ser2 proteins as major sericin components in the non-cocoon silk of Bombyx mori. Insect Biochemistry and Molecular Biology, 40, 339-344.
Takasu, Y., Yamada, H., Tamura, T., Sezutsu, H., Mita, K. and Tsubouchi, K. (2007) Identification and characterization of a novel sericin gene expressed in the anterior middle silk gland of the silkworm Bombyx mori. Insect Biochemistry and Molecular Biology, 37, 1234-1240.
Takiya, S., Tsubota, T. and Kimoto, M. (2016) Regulation of silk genes by Hox and homeodomain proteins in the terminal differentiated silk gland of the silkworm Bombyx mori. Journal of Developmental Biology, 4, 19.
Tamura, T. and Kubota, T. (1989) A determination of molecular weight of fibroin polypeptides in the saturnid silkworms, Antheraea yamamai, Antheraea pernyi and Philosamia cynthia ricini by SDS PAGE. Wild Silkmoth ’88 (eds. H. Akai & M. Kiguchi), pp. 67-72. National Institute of Sericultural and Insect Science, Tsukuba.
Tanaka, K., Inoue, S. and Mizuno, S. (1999a) Hydrophobic interaction of P25, containing Asn-linked oligosaccharide chains, with the H-L complex of silk fibroin produced by Bombyx mori. Insect Biochemistry and Molecular Biology, 29, 269-276.
Tanaka, K., Kajiyama, N., Ishikura, K., Waga, S., Kikuchi, A., Ohtomo, K. et al. (1999b) Determination of the site of disulfide linkage between heavy and light chains of silk fibroin produced by Bombyx mori. Biochimica et Biophysica Acta, 1432, 92-103.
Tanaka, K. and Mizuno, S. (2001) Homologues of fibroin L-chain and P25 of Bombyx mori are present in Dendrolimus spectabilis and Papilio xuthus but not detectable in Antheraea yamamai. Insect Biochemistry and Molecular Biology, 31, 665-677.
Tsubota, T., Tomita, S., Uchino, K., Kimoto, M., Takiya, S., Kajiwara, H. et al. (2016a) A Hox gene, Antennapedia, regulates expression of multiple major silk protein genes in the silkworm Bombyx mori. The Journal of Biological Chemistry, 291, 7087-7096.
Tsubota, T., Yamamoto, K., Mita, K. and Sezutsu, H. (2016b) Gene expression analysis in the larval silk gland of the eri silkworm Samia ricini. Insect Science, 23, 791-804.
Xia, Q., Cheng, D., Duan, J., Wang, G., Cheng, T., Zha, X. et al. (2007) Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biology, 8, R162.
Yonemura, N. and Sehnal, F. (2006) The design of silk fiber composition in moths has been conserved for more than 150 million years. Journal of Molecular Evolution, 63, 42-53.
Yoshioka, T., Tsubota, T., Tashiro, K., Jouraku, A. and Kameda, T. (2019) A study of the extraordinarily strong and tough silk produced by bagworms. Nature Communications, 10, 1469.
Yukuhiro, K., Sezutsu, H., Tsubota, T., Takasu, Y., Kameda, T. and Yonemura, N. (2016) Insect silks and cocoons: structural and molecular aspects. Extracellular Composite Matrices in Arthropods (eds. E. Cohen & B. Moussian), pp. 515-555. Springer, Cham.
Zhang, Y., Zhao, P., Dong, Z., Wang, D., Guo, P., Guo, X. et al. (2015) Comparative proteome analysis of multi-layer cocoon of the silkworm, Bombyx mori. PLoS ONE, 10, e0123403.
Zhou, C.Z., Confalonieri, F., Medina, N., Zivanovic, Y., Esnault, C., Yang, T. et al. (2001) Fine organization of Bombyx mori fibroin heavy chain gene. Nucleic Acids Research, 28, 2413-2419.
Žurovec, M., Kludkiewicz, B., Fedic, R., Sulitkova, J., Mach, V., Kucerova, L. et al. (2013) Functional conservation and structural diversification of silk sericins in two moth species. Biomacromolecules, 14, 1859-1866.
Žurovec, M. and Sehnal, F. (2002) Unique molecular architecture of silk fibroin in the waxmoth, Galleria mellonella. The Journal of Biological Chemistry, 277, 22639-22647.
Žurovec, M., Yonemura, N., Kludkiewicz, B., Sehnal, F., Kodrik, D., Vieira, L.C. et al. (2016) Sericin composition in the silk of Antheraea yamamai. Biomacromolecules, 17, 1776-1787.