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Large scale full-length cDNA sequencing reveals a unique genomic landscape in a lepidopteran model insect, Bombyx mori.

Suetsugu Y, Futahashi R, Kanamori H, Kadono-Okuda K, Sasanuma S, Narukawa J, Ajimura M, Jouraku A, Namiki N, Shimomura M, Sezutsu H, Osanai-Futahashi M, Suzuki MG, Daimon T, Shinoda T, Taniai K, Asaoka K, Niwa R, Kawaoka S, Katsuma S, Tamura T, Noda H, Kasahara M, Sugano S, Suzuki Y, Fujiwara H, Kataoka H, Arunkumar KP, Tomar A, Nagaraju J, Goldsmith MR, Feng Q, Xia Q, Yamamoto K, Shimada T, Mita K - G3 (Bethesda) (2013)

Bottom Line: The establishment of a complete genomic sequence of silkworm, the model species of Lepidoptera, laid a foundation for its functional genomics.More than 40% of genes expressed in specific tissues mapped in tissue-specific chromosomal clusters.The newly obtained FL-cDNA sequences enabled us to annotate the genome of this lepidopteran model insect more accurately, enhancing genomic and functional studies of Lepidoptera and comparative analyses with other insect orders, and yielding new insights into the evolution and organization of lepidopteran-specific genes.

View Article: PubMed Central - PubMed

Affiliation: National Institute of Agrobiological Sciences, Tsukuba 305-8634, Japan.

ABSTRACT
The establishment of a complete genomic sequence of silkworm, the model species of Lepidoptera, laid a foundation for its functional genomics. A more complete annotation of the genome will benefit functional and comparative studies and accelerate extensive industrial applications for this insect. To realize these goals, we embarked upon a large-scale full-length cDNA collection from 21 full-length cDNA libraries derived from 14 tissues of the domesticated silkworm and performed full sequencing by primer walking for 11,104 full-length cDNAs. The large average intron size was 1904 bp, resulting from a high accumulation of transposons. Using gene models predicted by GLEAN and published mRNAs, we identified 16,823 gene loci on the silkworm genome assembly. Orthology analysis of 153 species, including 11 insects, revealed that among three Lepidoptera including Monarch and Heliconius butterflies, the 403 largest silkworm-specific genes were composed mainly of protective immunity, hormone-related, and characteristic structural proteins. Analysis of testis-/ovary-specific genes revealed distinctive features of sexual dimorphism, including depletion of ovary-specific genes on the Z chromosome in contrast to an enrichment of testis-specific genes. More than 40% of genes expressed in specific tissues mapped in tissue-specific chromosomal clusters. The newly obtained FL-cDNA sequences enabled us to annotate the genome of this lepidopteran model insect more accurately, enhancing genomic and functional studies of Lepidoptera and comparative analyses with other insect orders, and yielding new insights into the evolution and organization of lepidopteran-specific genes.

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Synteny of the osiris gene cluster between silkworm and fruitfly. Green, osiris genes transcribed only in wing; red, osiris genes transcribed in several tissues; black, osiris genes with no evidence for transcription. Silkworm osiris genes are numbered according to the Drosophila gene set; (+) and (–) denote the orientation of the gene.
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fig5: Synteny of the osiris gene cluster between silkworm and fruitfly. Green, osiris genes transcribed only in wing; red, osiris genes transcribed in several tissues; black, osiris genes with no evidence for transcription. Silkworm osiris genes are numbered according to the Drosophila gene set; (+) and (–) denote the orientation of the gene.

Mentions: Osiris genes are highly conserved and clustered in insects; however, their function is still unknown (Dorer et al. 2003; Shah et al. 2012). Interestingly, we found several wing-specific osiris genes in B. mori that were clustered on ch.26. Among them we could identify several Drosophila osiris homologs, although some of them were missing from the silkworm genome, including Osi1, Osi4-6, Osi13-15, and Osi23. It was reported that Drosophila osiris genes encode a novel family of transmembrane proteins (Dorer et al. 2003), all of which contain a well-conserved pair of cysteine amino acid residues. Using the protein structure prediction programs PSORT (Nakai and Horton 1999) and SOSUI (Hirokawa et al. 1998), we found silkworm osiris proteins had the same structural features. Bmosi2 and Bmosi16 provided no evidence for transcription and may be pseudogenes or misannotated. Although we found no silkworm homologs to Drosophila osiris genes 4−6 and 13−15, the remainder of Bmosi3–Bmosi18 were clustered in a single locus of ch.26:11,546,404-11,956,406 in the same order as Drosophila osiris genes 1-20 (Figure 5; Table S4). In addition, five copies of Bmosi9 were found in a cluster between Bmosi7 and Bmosi8 in the region ch26:11,684,158-11,776,381. By phylogenetic analysis, these 5 copies were formed by gene duplication events after separation of Lepidoptera from Diptera. The homologs of Dmosi21 and 22 were unlinked to the main silkworm osiris gene cluster on ch. 26, which was consistent with their independent genetic linkage mapping on ch.4 and ch.12, respectively. These results indicate an explicit microsynteny between silkworm and fruitfly genomes (Figure 5).


Large scale full-length cDNA sequencing reveals a unique genomic landscape in a lepidopteran model insect, Bombyx mori.

Suetsugu Y, Futahashi R, Kanamori H, Kadono-Okuda K, Sasanuma S, Narukawa J, Ajimura M, Jouraku A, Namiki N, Shimomura M, Sezutsu H, Osanai-Futahashi M, Suzuki MG, Daimon T, Shinoda T, Taniai K, Asaoka K, Niwa R, Kawaoka S, Katsuma S, Tamura T, Noda H, Kasahara M, Sugano S, Suzuki Y, Fujiwara H, Kataoka H, Arunkumar KP, Tomar A, Nagaraju J, Goldsmith MR, Feng Q, Xia Q, Yamamoto K, Shimada T, Mita K - G3 (Bethesda) (2013)

Synteny of the osiris gene cluster between silkworm and fruitfly. Green, osiris genes transcribed only in wing; red, osiris genes transcribed in several tissues; black, osiris genes with no evidence for transcription. Silkworm osiris genes are numbered according to the Drosophila gene set; (+) and (–) denote the orientation of the gene.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3755909&req=5

fig5: Synteny of the osiris gene cluster between silkworm and fruitfly. Green, osiris genes transcribed only in wing; red, osiris genes transcribed in several tissues; black, osiris genes with no evidence for transcription. Silkworm osiris genes are numbered according to the Drosophila gene set; (+) and (–) denote the orientation of the gene.
Mentions: Osiris genes are highly conserved and clustered in insects; however, their function is still unknown (Dorer et al. 2003; Shah et al. 2012). Interestingly, we found several wing-specific osiris genes in B. mori that were clustered on ch.26. Among them we could identify several Drosophila osiris homologs, although some of them were missing from the silkworm genome, including Osi1, Osi4-6, Osi13-15, and Osi23. It was reported that Drosophila osiris genes encode a novel family of transmembrane proteins (Dorer et al. 2003), all of which contain a well-conserved pair of cysteine amino acid residues. Using the protein structure prediction programs PSORT (Nakai and Horton 1999) and SOSUI (Hirokawa et al. 1998), we found silkworm osiris proteins had the same structural features. Bmosi2 and Bmosi16 provided no evidence for transcription and may be pseudogenes or misannotated. Although we found no silkworm homologs to Drosophila osiris genes 4−6 and 13−15, the remainder of Bmosi3–Bmosi18 were clustered in a single locus of ch.26:11,546,404-11,956,406 in the same order as Drosophila osiris genes 1-20 (Figure 5; Table S4). In addition, five copies of Bmosi9 were found in a cluster between Bmosi7 and Bmosi8 in the region ch26:11,684,158-11,776,381. By phylogenetic analysis, these 5 copies were formed by gene duplication events after separation of Lepidoptera from Diptera. The homologs of Dmosi21 and 22 were unlinked to the main silkworm osiris gene cluster on ch. 26, which was consistent with their independent genetic linkage mapping on ch.4 and ch.12, respectively. These results indicate an explicit microsynteny between silkworm and fruitfly genomes (Figure 5).

Bottom Line: The establishment of a complete genomic sequence of silkworm, the model species of Lepidoptera, laid a foundation for its functional genomics.More than 40% of genes expressed in specific tissues mapped in tissue-specific chromosomal clusters.The newly obtained FL-cDNA sequences enabled us to annotate the genome of this lepidopteran model insect more accurately, enhancing genomic and functional studies of Lepidoptera and comparative analyses with other insect orders, and yielding new insights into the evolution and organization of lepidopteran-specific genes.

View Article: PubMed Central - PubMed

Affiliation: National Institute of Agrobiological Sciences, Tsukuba 305-8634, Japan.

ABSTRACT
The establishment of a complete genomic sequence of silkworm, the model species of Lepidoptera, laid a foundation for its functional genomics. A more complete annotation of the genome will benefit functional and comparative studies and accelerate extensive industrial applications for this insect. To realize these goals, we embarked upon a large-scale full-length cDNA collection from 21 full-length cDNA libraries derived from 14 tissues of the domesticated silkworm and performed full sequencing by primer walking for 11,104 full-length cDNAs. The large average intron size was 1904 bp, resulting from a high accumulation of transposons. Using gene models predicted by GLEAN and published mRNAs, we identified 16,823 gene loci on the silkworm genome assembly. Orthology analysis of 153 species, including 11 insects, revealed that among three Lepidoptera including Monarch and Heliconius butterflies, the 403 largest silkworm-specific genes were composed mainly of protective immunity, hormone-related, and characteristic structural proteins. Analysis of testis-/ovary-specific genes revealed distinctive features of sexual dimorphism, including depletion of ovary-specific genes on the Z chromosome in contrast to an enrichment of testis-specific genes. More than 40% of genes expressed in specific tissues mapped in tissue-specific chromosomal clusters. The newly obtained FL-cDNA sequences enabled us to annotate the genome of this lepidopteran model insect more accurately, enhancing genomic and functional studies of Lepidoptera and comparative analyses with other insect orders, and yielding new insights into the evolution and organization of lepidopteran-specific genes.

Show MeSH
Related in: MedlinePlus