Comparative Analysis of Transcriptomes among Bombyx mori Strains and Sexes Reveals the Genes Regulating Melanic Morph and the Related Phenotypes

PLOS ONE, Dec 2019

As a source of insect polymorphism, melanism plays an important role in ecological adaption and usually endows advantageous phenotypic-effects on insects. However, due to the mechanistic diversity, there are knowledge gaps in the molecular mechanisms underlying melanism and the related phenotypes. In silk moths, a recessive melanic mutant (sex-controlled melanism, sml) strain exhibits extended adult longevity. We took a transcriptome approach to perform a comparative analysis between this sml strain and a wild-type strain (Dazao). Our analysis resulted in the identification of 59 unique differentially expressed genes in the melanic mutant. Two key genes (laccase2 and yellow) involved in melanin formation were significantly up-regulated in melanic individuals. The laccase2 B-type isoform (BGIBMGA006746) was found to likely participate in the silkworm cuticular melanism process at late pupal stage. Moreover, we discovered 22 cuticular protein encoding genes with the possible function in melanin transport and/or maintenance. Based on our findings, we presume that the longer survival of the melanic sml male moths might be associated with the enhanced antioxidant defense systems and a reduction in the insulin/IGF-1 signaling pathway (IIS). These findings will facilitate the understanding of the molecular basis underlying melanism and the derived phenotypic-effects.

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Comparative Analysis of Transcriptomes among Bombyx mori Strains and Sexes Reveals the Genes Regulating Melanic Morph and the Related Phenotypes

May Comparative Analysis of Transcriptomes among Bombyx mori Strains and Sexes Reveals the Genes Regulating Melanic Morph and the Related Phenotypes Songzhen He 0 1 2 Xiaoling Tong 0 1 2 Kunpeng Lu 0 1 2 Yaru Lu 0 1 2 Jiangwen Luo 0 1 2 Wenhao Yang 0 1 2 Min Chen 0 1 2 Min-jin Han 0 1 2 Hai Hu 0 1 2 Cheng Lu 0 1 2 Fangyin Dai 0 1 2 0 State Key Laboratory of Silkworm Genome Biology, Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry, Southwest University , Chongqing, 400715 , China 1 Science Foundation of China (No. 31372379, No. 31472153) , Hi-Tech Research and Development 863 Program of China Grant (No. 2013AA102507), and Chongqing Youth Science and Technology Talent Training Project (cstc2014kjrc-qnrc80001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript 2 Editor: Erjun Ling, Institute of Plant Physiology and Ecology , CHINA As a source of insect polymorphism, melanism plays an important role in ecological adaption and usually endows advantageous phenotypic-effects on insects. However, due to the mechanistic diversity, there are knowledge gaps in the molecular mechanisms underlying melanism and the related phenotypes. In silk moths, a recessive melanic mutant (sex-controlled melanism, sml) strain exhibits extended adult longevity. We took a transcriptome approach to perform a comparative analysis between this sml strain and a wild-type strain (Dazao). Our analysis resulted in the identification of 59 unique differentially expressed genes in the melanic mutant. Two key genes (laccase2 and yellow) involved in melanin formation were significantly up-regulated in melanic individuals. The laccase2 B-type isoform (BGIBMGA006746) was found to likely participate in the silkworm cuticular melanism process at late pupal stage. Moreover, we discovered 22 cuticular protein encoding genes with the possible function in melanin transport and/or maintenance. Based on our findings, we presume that the longer survival of the melanic sml male moths might be associated with the enhanced antioxidant defense systems and a reduction in the insulin/IGF-1 signaling pathway (IIS). These findings will facilitate the understanding of the molecular basis underlying melanism and the derived phenotypic-effects. - OPEN ACCESS Data Availability Statement: All raw data files are available from the NCBI Short Read Archive database (accession number: SRR3068622). Introduction Pigmentation plays an important role in the adaptive processes of insects and provides a model system for biology [ 1,2 ]. One of the most common primary pigmentation processes is melanism, which occurs throughout Insecta and is an important source of insect polymorphism [ 3– 7 ]. It is caused by the accumulation of melanin [ 4,8 ], and the genes, proteins and metabolites pertaining to melanin metabolism pathway in insects have been extensively studied [ 8,9 ]. Functional defects or abnormal expression of some key genes in the melanin metabolism Competing Interests: The authors have declared that no competing interests exist. pathway can also lead to melanism [ 6,9,10 ]. In contrast, some studies found that some melanic morphs had no variations in the classic melanin metabolism pathway genes indicating the mechanistic diversity of melanism [ 7,11,12 ]. An example for this mechanism is the industrial melanism in the peppered moth (Biston betularia) [ 7,11 ]. These studies suggest a knowledge gap in the genetic basis and regulatory mechanism of insect melanism. In addition to insect polymorphism, melanism also plays an important role in ecological adaption. For example, in numerous cases, melanism is associated with advantageous phenotypes, such as higher fecundity, increased pathogen resistance, higher vigor, higher resistance to UV, etc. [ 2,13–18 ]. Deciphering the molecular basis underlying the relationship between melanism and the related phenotypic-effects could complement our existing knowledge in ecological mechanisms related to melanism, and clarify potential mechanisms in adaptive evolution. The silkworm, Bombyx mori, is the most advanced lepidopteran model with over 100 body color mutants described thus far [ 19,20 ]. Studies of body color mutants has enhanced our fundamental understanding of the silkworm pigmentation processes and the genetic mechanisms underlying insect melanism [ 6,10,12,21–25 ]. Recently, a new melanic mutant in the silk moths termed sex-controlled melanism (sml) was discovered by researchers in the Silkworm Gene Bank of Southwest University, China [ 26 ]. It is a spontaneous autosomal recessive mutant [ 26 ], and has a rare wing- and body-color variation in adult B. mori. The sml female moths exhibit the white appearance of typical wild-types and are without obvious abnormal phenotypes, while the sml male moths exhibit the melanic phenotype, and interestingly also show extended adult (...truncated)


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Songzhen He, Xiaoling Tong, Kunpeng Lu, Yaru Lu, Jiangwen Luo, Wenhao Yang, Min Chen, Min-jin Han, Hai Hu, Cheng Lu, Fangyin Dai. Comparative Analysis of Transcriptomes among Bombyx mori Strains and Sexes Reveals the Genes Regulating Melanic Morph and the Related Phenotypes, PLOS ONE, 2016, Volume 11, Issue 5, DOI: 10.1371/journal.pone.0155061