BmCHSA-2b, a Lepidoptera specific alternative splicing variant of epidermal chitin synthase, is required for pupal wing development in Bombyx mori

Xu, Guanfeng; Zhang, Jie; Lyu, Hao; Liu, Jia; Ding, Yang; Feng, Qili; Song, Qisheng; Zheng, Sichun

doi:10.1016/j.ibmb.2017.06.017

Cited by 17 publications

(16 citation statements)

References 29 publications

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“…Xu et al . () confirmed that BmCHSA‐2b is necessary for wing development in the B. mori mid‐pupa. The minute wing mutant ( Bm‐mw ) in silkworm was mapped to a 275 kb region on chromosome 22 between marker T2272 and the end of nscaf3056 (Ma et al ., ), and a palmitoyltransferase approximated gene ( Bm‐app ) was identified as the candidate gene for the Bm‐mw mutant (Yu et al ., ).…”

Section: Introductionmentioning

confidence: 57%

BmSd gene regulates the silkworm wing size by affecting the Hippo pathway

Yin

Zhang

et al. 2019

Insect Science

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Insect wings are developed from the wing disc during metamorphosis. Bombyx mori, a model lepidopteran insect, loses flight ability after long-term domestication from the wild silkworm, Bombyx mandarina. The mw mutant (u11 strain) shows minute wings compared to wild type (e.g., p50 strain) wings. RNA sequencing analysis previously revealed differential Hippo-pathway-related gene expression between the u11 and p50 strains. The Hippo pathway is an evolutionarily conserved signaling cascade that controls organ size during development in animals. In this study, the function of BmSd which has been characterized as one of the Hippo-pathway-related genes was analyzed for silkworm wing development. We found that mats, warts, and hippo expression levels were higher in u11 compared to p50 wing discs. BmSd (scalloped) expression, which encodes a prominent transcriptional partner to Yorkie (Yki), gradually decreased during the wandering stage in u11, but exhibited the opposite expression pattern in p50. When BmSd was knocked down by small interfering RNA during the wandering stage in the p50 strain, 57.9% of the individuals showed minute wings. Additionally, ex, kibra, and wingless expression levels decreased in the BmSd knockdown mutant. Further, BmSd deletion mediated by clustered regularly interspaced short palindromic repeats (CRISPR) / CRISPR-associated protein 9 induced 50% of individuals with minute wings, a phenotype similar to the mw mutant. This result demonstrates that BmSd plays pivotal roles in silkworm wing development. Our results show that the Hippo signaling pathway participates and plays crucial roles in the regulation of silkworm wing development, and our findings provide a basis for further research on B. mori wing development.

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Section: Introductionmentioning

confidence: 57%

BmSd gene regulates the silkworm wing size by affecting the Hippo pathway

Yin

Zhang

et al. 2019

Insect Science

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“…Bombyx mori BmCHSA - 2b is a tissue- and stage-specifically expressed gene and expressed only in the pupal wings, not in the epidermis [ 23 ]. What controls this high specificity is extremely important for the development progress and, therefore, is interesting.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, probably in both insects and mammals, DNA methylation in the intragenic promoter functions as a suppressor to control tissue-specific gene expression. This different effect of intragenic DNA methylation on BmCHSA - 2a and BmCHSA - 2b transcription is coincidence with their expression patterns: BmCHSA - 2a is expressed in pupal wings as well as epidermis while BmCHSA - 2b is specifically expressed in pupal wings [ 23 ]. Similar CHSA gene structure was also found in other Lepidoptera , for example, Spodoptera litura SlCHSA [ 23 ] .…”

Section: Discussionmentioning

confidence: 99%

“…Two alternative splicing variants of BmCHSA , BmCHSA - 2a and BmCHSA - 2b were up-regulated in the beginning and middle of pupal wing, driven by two different promoters, respectively. BmCHSA - 2b RNAi resulted in the undeveloped wing [ 23 ]. The intragenic promoter that activates the tissue- and stage-specific expression of BmCHSA - 2b is located between exon 2a and exon 2b of BmCHSA [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

“…BmCHSA - 2b RNAi resulted in the undeveloped wing [ 23 ]. The intragenic promoter that activates the tissue- and stage-specific expression of BmCHSA - 2b is located between exon 2a and exon 2b of BmCHSA [ 23 ]. We hypothesized that intragenic promoter methylation mediates the tissue-specific expression of BmCHSA - 2b .…”

Section: Introductionmentioning

confidence: 99%

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DNA methylation mediates BmDeaf1-regulated tissue- and stage-specific expression of BmCHSA-2b in the silkworm, Bombyx mori

Zhang

Lyu

et al. 2018

Epigenetics & Chromatin

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BackgroundAccurate regulation of tissue- and stage-specific expression of genes is prerequisite for normal development in organisms. DNA methylation plays an important role in modulating gene expression in mammals and plants. However, there is no direct evidence showing how DNA methylation regulates gene transcription in insects.ResultsDuring the development of Bombyx mori wing, the expression level of DNA methyltransferase 1 (BmDnmt1) gradually declined and became stationary at pupal stage, resulting in a lower methylation rate of the intragenic promoter of the mid-pupal wing-specific gene BmCHSA-2b, an epidermal chitin synthase controlling mid-pupal wing development in B. mori. The higher methylation rate of the promoter in the pupal epidermis was decreased and BmCHSA-2b transcription was significantly increased by the treatment with the DNA methylation inhibitor, 5-azacytidine-2′-deoxycytidine, suggesting that DNA methylation regulates the tissue-specific expression of BmCHSA-2b. Pupa-specific transcription factor BmDEAF1 bound to the unmethylated intragenic promoter and activated the BmCHSA-2b transcription in the mid-pupal wing. BmDnmt1 and BmDeaf1 influenced the BmCHSA-2b transcription by binding competitively to the CpG island in the promoter.ConclusionsAll the data together demonstrate that the cooperation between the down-regulation of BmDnmt1 and increased stage-specific expression of BmDeaf1 enhances BmCHSA-2b tissue- and stage-specific transcription to ensure mid-wing development in B. mori. This study highlights an elaborate regulation mechanism how tissue- and stage-specific gene expression is regulated through promoter methylation in insect development.Electronic supplementary materialThe online version of this article (10.1186/s13072-018-0202-4) contains supplementary material, which is available to authorized users.

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