Comparative transcriptome analyses on silk glands of six silkmoths imply the genetic basis of silk structure and coloration

Dong et al. BMC Genomics Comparative transcriptome analyses on silk glands of six silkmoths imply the genetic basis of silk structure and coloration Yang Dong 0 Fangyin Dai Yandong Ren 0 Hui Liu 0 Lei Chen 0 Pengcheng Yang Yanqun Liu Xin Li Wen Wang 0 Hui Xiang 0 0 State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences , 32 East Jiaochang Road, Kunming, Yunnan Province 650223 , China Background: Silk has numerous unique properties that make it a staple of textile manufacturing for several thousand years. However, wider applications of silk in modern have been stalled due to limitations of traditional silk produced by Bombyx mori. While silk is commonly produced by B. mori, several wild non-mulberry silkmoths- -especially members of family Saturniidae- -produce silk with superior properties that may be useful for wider applications. Further utilization of such silks is hampered by the non-domestication status or limited culturing population of wild silkworms. To date there is insufficient basic genomic or transcriptomic data on these organisms or their silk production. Results: We sequenced and compared the transcriptomes of silk glands of six Saturniidae wild silkmoth species through next-generation sequencing technology, identifying 37758 ~ 51734 silkmoth unigenes, at least 36.3% of which are annotated with an e-value less than 105. Sequence analyses of these unigenes identified a batch of genes specific to Saturniidae that are enriched in growth and development. Analyses of silk proteins including fibroin and sericin indicate intra-genus conservation and inter-genus diversification of silk protein features among the wild silkmoths, e.g., isoelectric points, hydrophilicity profile and amino acid composition in motifs of silk H-fibroin. Interestingly, we identified p25 in two of the silkmoths, which were previously predicted to be absent in Saturniidae. There are rapid evolutionary changes in sericin proteins, which might account for the highly heterogeneity of sericin in Saturniidae silkmoths. Within the six sikmoths, both colored-cocoon silkmoth specific transcripts and differentially expressed genes between the colored-cocoon and non-colored-cocoon silkmoths are significantly enriched in catalytic activity, especially transferase activity, suggesting potentially viable targets for future gene mining or genetic manipulation. Conclusions: Our results characterize novel and potentially valuable gene resources of saturniid silkmoths that may facilitate future genetic improvement and modification of mulberry silkworms. Our results suggest that the disparate features of silk- -coloration, retention, strength, etc. - -are likely not only due to silk proteins, but also to the environment of silk assembly, and more specifically, that stable silk coloration exhibited by some Saturniidae silkmoths may be attributable to active catalytic progress in pigmentation. Silkmoths; Comparative transcriptomics; Silk proteins; Silk coloration - Background Functional genomics has yielded an abundance of data on numerous plant and animal species while also providing novel techniques for isolating valuable traits or genes from these organisms. Further application of these techniques to economically valuable species holds the potential to vastly improve the quality of their produce by offering directions into future gene mining, genetic manipulation or breeding efforts. For example, silk produced by silkworms has long held historical, economic and cultural significance worldwide, especially in China where the mulberry silkworm Bombyx mori (B. mori) was domesticated nearly 5000 years ago. Today, China remains the worlds largest producer and exporter of B. mori cocoons and raw silks, which are predominately used textile manufacturing. Advances in genomics and material sciences have also suggested potential uses of silk in medicine and security biomaterials, but several hurdles remain to these nontraditional applications, not the least of which being that the silk commonly produced from B. mori is less than ideal for such novel purposes or even more advanced silk textile production. For instance, B. mori silk has weak color retention, making it difficult to satisfy consumers textile demands; while outside of textiles utilization of this silk cannot meet tensile strength well for industrial application or use as a biomaterial. However, silk produced from other organisms often possess one or more of superior characteristics not present in B. mori silk, but these organisms silk production is poorly understood due to lack of genomic and genetic data. Aside from B. mori, several wild non-mulberry silkmoths, especially members of family Saturniidae, produce silks with unique features that are well suited to novel applications both within and outside of textiles. The family Saturniidaethe largest and arguably most spectacular in Lepidopterais comprised of over 1,500 different species [1], including economically important silk-producing moths such as Chinese and Japanese oak moth (Antheraea pernyi and A. yamamai), Assam silkmoth (A. assama) and Eri silkmoth (Samia Cynthia ricini). Of these, the yield of A. pernyi silk is next to that of B. mori, while the silk of A. yamamai and A. assama remains among the most valuable and expensive, being only used in top-end textiles due to its superior natural colors. Silk from S. cynthia is widely used in conjunction with cotton, hemp, wool or chemical fiber to create blended fabric. Likewise, other silk-producers such as Actias selene (Ac. selene) and Rhodinia newara possess unique characteristics with economic potential. Structurally, silk glands of Saturniidae species are morphologically distinctive from those of B. mori. The former glands have relatively uniform curved morphology with no obvious distinction between the middle and posterior regions of the silk-glands, whereas the latter show drastic differences between the two regions, with the mid-silk glands swelling and straight and the posterior silk glands being curved [2]. Likely due to the morphological differences as well as differences in genetics and the underlying molecular structure of silk producing glands, silk produced by these Saturniidae species generally exhibits unique properties in terms of color, luster, strength, biological compatibility and cell adhesiveness, which either alone or in tandem make them commercially attractive for certain existing uses (i.e., textiles) or novel applications in medical applications [3,4]. In particular, silk from Antheraea moths such as A. pernyi, A. yamamai and A. assama, as well as Ac. selene and R. fugax, all share a markedly better tenacity, tensile strength and general toughness as compared to B. mori. R. newara, another species in the genus Rhodinia, has the nearly same cocoon features as those from of R. fugax. While the silk of S. cynthia has a weak tensile strength (making it diff (...truncated)