Turn off MathJax
Article Contents
Han Xu, Lei Chen, Xiao-Ling Tong, Hai Hu, Li-Yuan Liu, Gui-Chun Liu, Ya-Nan Zhu, Ruo-Ping Zhao, Wen Wang, Fang-Yin Dai, Xin Li, Hui Xiang. Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis. Zoological Research, 2022, 43(4): 585-596. doi: 10.24272/j.issn.2095-8137.2022.065
Citation: Han Xu, Lei Chen, Xiao-Ling Tong, Hai Hu, Li-Yuan Liu, Gui-Chun Liu, Ya-Nan Zhu, Ruo-Ping Zhao, Wen Wang, Fang-Yin Dai, Xin Li, Hui Xiang. Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis. Zoological Research, 2022, 43(4): 585-596. doi: 10.24272/j.issn.2095-8137.2022.065

Comprehensive silk gland multi-omics comparison illuminates two alternative mechanisms in silkworm heterosis

doi: 10.24272/j.issn.2095-8137.2022.065
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (31371286, 32070411, 81872299, 31830094, U20A2058), Guangzhou Science Technology Project (201904010007), Shenzhen Science and Technology Program (JCYJ20190807160011600, JCYJ20210324124808023), and Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology (GDKCFY2101)
More Information
  • Heterosis is a common phenomenon in plants and animals with diverse underlying mechanisms. Here, we applied two widely used silkworm hybrid systems and performed multi-omics analysis to identify possible intrinsic associations between different hybrid strategies and epigenetic mechanisms with silkworm heterosis. We found significant differences in the silk gland transcriptomic landscape between the two systems, including differentially expressed genes and expression patterns in the hybrid offspring compared to their parents. In the quaternary hybrid system, hybrid vigor was primarily due to up-regulated genes and the parent-dominant up-regulated expression pattern, involving multiple transport processes, cellular nitrogen compound catabolism, glucose metabolism, and tricarboxylic acid cycle. In the binary system, hybrid vigor was mainly due to the down-regulated genes and transgressively down-regulated expression pattern, mainly involving basic nitrogen synthesis metabolism and body function. We also demonstrated that DNA methylation may affect hybrid vigor by regulating the expression of several heterosis-related genes. Thus, this study revealed two alternative mechanisms that may contribute to silkworm heterosis, both of which facilitate the efficient utilization of energy and nitrogen for silk production.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Adolf F, Rhiel M, Hessling B, Gao Q, Hellwig A, Béthune J, et al. 2019. Proteomic profiling of mammalian COPII and COPI vesicles. Cell Reports, 26(1): 250−265.e5. doi: 10.1016/j.celrep.2018.12.041
    Akram M. 2014. Citric acid cycle and role of its intermediates in metabolism. Cell Biochemistry and Biophysics, 68(3): 475−478. doi: 10.1007/s12013-013-9750-1
    Arakel EC, Schwappach B. 2018. Formation of COPI-coated vesicles at a glance. Journal of Cell Science, 131(5): jcs209890. doi: 10.1242/jcs.209890
    Bastiani MJ, De Couet HG, Quinn JMA, Karlstrom RO, Kotrla K, Goodman CS, et al. 1992. Position-specific expression of the annulin protein during grasshopper embryogenesis. Developmental Biology, 154(1): 129−142. doi: 10.1016/0012-1606(92)90054-K
    Béthune J, Wieland FT. 2018. Assembly of COPI and COPII vesicular coat proteins on membranes. Annual Review of Biophysics, 47: 63−83. doi: 10.1146/annurev-biophys-070317-033259
    Birchler JA, Auger DL, Riddle NC. 2003. In search of the molecular basis of heterosis. The Plant Cell, 15(10): 2236−2239. doi: 10.1105/tpc.151030
    Birchler JA, Yao H, Chudalayandi S. 2006. Unraveling the genetic basis of hybrid vigor. Proceedings of the National Academy of Sciences of the United States of America, 103(35): 12957−12958. doi: 10.1073/pnas.0605627103
    Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15): 2114−2120. doi: 10.1093/bioinformatics/btu170
    Børsheim E, Cree MG, Tipton KD, Elliott TA, Aarsland A, Wolfe RR. 2004. Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. Journal of Applied Physiology, 96(2): 674−678. doi: 10.1152/japplphysiol.00333.2003
    Chen ZJ. 2013. Genomic and epigenetic insights into the molecular bases of heterosis. Nature Reviews Genetics, 14(7): 471−482. doi: 10.1038/nrg3503
    Cui Y, Liu ZL, Li CC, Wei XM, Lin YJ, You L, et al. 2021. Role of juvenile hormone receptor Methoprene-tolerant 1 in silkworm larval brain development and domestication. Zoological Research, 42(5): 637−649. doi: 10.24272/j.issn.2095-8137.2021.126
    Davenport CB. 1908. Degeneration, albinism and inbreeding. Science, 28(718): 454−455. doi: 10.1126/science.28.718.454.a
    Depristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics, 43(5): 491−498. doi: 10.1038/ng.806
    Dyer WTT. 1877. The effects of cross and self-fertilisation in the vegetable kingdom. Nature, 15(381): 329−332. doi: 10.1038/015329a0
    East EM. 1936. Heterosis. Genetics, 21(4): 375−397. doi: 10.1093/genetics/21.4.375
    Feng Y, Lei X, Zhang L, Wan H, Pan H, Wu J, et al. 2021. COPB2: a transport protein with multifaceted roles in cancer development and progression. Clinical and Translational Oncology, 23(11): 2195−2205. doi: 10.1007/s12094-021-02630-9
    Fu DH, Xiao ML, Hayward A, Fu Y, Liu G, Jiang GJ, et al. 2014. Utilization of crop heterosis: a review. Euphytica, 197(2): 161−173. doi: 10.1007/s10681-014-1103-7
    Ge Q, Xiao R, Yuan Y, He SQ, Chen L, Ma SS, et al. 2020. Transcriptome and proteomics-based analysis to investigate the regulatory mechanism of silk gland differences between reciprocal cross silkworm. Bombyx mori. Journal of Asia-Pacific Entomology, 23(4): 1101−1113. doi: 10.1016/j.aspen.2020.09.002
    Goddard ME. 2012. Uses of genomics in livestock agriculture. Animal Production Science, 52(3): 73−77. doi: 10.1071/AN11180
    Guo M, Yang SA, Rupe M, Hu B, Bickel DR, Arthur L, et al. 2008. Genome-wide allele-specific expression analysis using massively parallel signature sequencing (MPSSTM) reveals cis-and trans-effects on gene expression in maize hybrid meristem tissue. Plant Molecular Biology, 66(5): 551−563. doi: 10.1007/s11103-008-9290-z
    Hirayama C, Konno K, Shinbo H. 1997. The pathway of ammonia assimilation in the silkworm. Bombyx mori. Journal of Insect Physiology, 43(10): 959−964. doi: 10.1016/S0022-1910(97)00045-0
    Hu XJ, Wang HW, Li K, Wu YJ, Liu ZF, Huang CL. 2017. Genome-wide proteomic profiling reveals the role of dominance protein expression in heterosis in immature maize ears. Scientific Reports, 7(1): 16130. doi: 10.1038/s41598-017-15985-3
    Kim D, Langmead B, Salzberg SL. 2015. HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 12(4): 357−360. doi: 10.1038/nmeth.3317
    Klosinska M, Picard CL, Gehring M. 2016. Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus. Nature Plants, 2(10): 16145.
    Kong XP, Chen L, Wei TZ, Zhou HW, Bai CF, Yan XP, et al. 2020. Transcriptome analysis of biological pathways associated with heterosis in Chinese cabbage. Genomics, 112(6): 4732−4741. doi: 10.1016/j.ygeno.2020.08.011
    Krieg UC, Johnson AE, Walter P. 1989. Protein translocation across the endoplasmic reticulum membrane: identification by photocross-linking of a 39-kD integral membrane glycoprotein as part of a putative translocation tunnel. The Journal of Cell Biology, 109(5): 2033−2043. doi: 10.1083/jcb.109.5.2033
    Krueger F, Andrews SR. 2011. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics, 27(11): 1571−1572. doi: 10.1093/bioinformatics/btr167
    Lauss K, Wardenaar R, Oka R, Van Hulten MHA, Guryev V, Keurentjes JJB, et al. 2018. Parental DNA methylation states are associated with heterosis in epigenetic hybrids. Plant Physiology, 176(2): 1627−1645. doi: 10.1104/pp.17.01054
    Lester DS, Gilbert LI. 1986. Developmental changes in choline uptake and acetylcholine metabolism in the larval brain of the tobacco hornworm. Manduca sexta. Developmental Brain Research, 26(2): 201−209. doi: 10.1016/0165-3806(86)90284-1
    Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25(14): 1754−1760. doi: 10.1093/bioinformatics/btp324
    Li H, Yuan JY, Wu M, Han ZP, Li LH, Jiang HM, et al. 2018. Transcriptome and DNA methylome reveal insights into yield heterosis in the curds of broccoli (Brassica oleracea L var. italic). BMC Plant Biology, 18(1): 168. doi: 10.1186/s12870-018-1384-4
    Li JY, Ye LP, Che JQ, Song J, You ZY, Yun KC, et al. 2015. Comparative proteomic analysis of the silkworm middle silk gland reveals the importance of ribosome biogenesis in silk protein production. Journal of Proteomics, 126: 109−120. doi: 10.1016/j.jprot.2015.06.001
    Li ZK, Luo LJ, Mei HW, Wang DL, Shu QY, Tabien R, et al. 2001. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics, 158(4): 1737−1753. doi: 10.1093/genetics/158.4.1737
    Lidén M, Eriksson U. 2006. Understanding retinol metabolism: structure and function of retinol dehydrogenases. Journal of Biological Chemistry, 281(19): 13001−13004. doi: 10.1074/jbc.R500027200
    Lister R, O'malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, et al. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell, 133(3): 523–536.
    Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature, 462(7271): 315−322. doi: 10.1038/nature08514
    Liu YJ, Gao SQ, Tang YM, Gong J, Zhang X, Wang YB, et al. 2018. Transcriptome analysis of wheat seedling and spike tissues in the hybrid Jingmai 8 uncovered genes involved in heterosis. Planta, 247(6): 1307−1321. doi: 10.1007/s00425-018-2848-3
    Luo JH, Wang M, Jia GF, He Y. 2021. Transcriptome-wide analysis of epitranscriptome and translational efficiency associated with heterosis in maize. Journal of Experimental Botany, 72(8): 2933−2946. doi: 10.1093/jxb/erab074
    McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ. 2010. Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Research, 20(6): 816−825. doi: 10.1101/gr.102491.109
    Metzler MA, Raja S, Elliott KH, Friedl RM, Tran NQH, Brugmann SA, et al. 2018. RDH10-mediated retinol metabolism and RARα-mediated retinoic acid signaling are required for submandibular salivary gland initiation. Development, 145(15): dev164822.
    Ni M, Li FC, Tian JH, Hu JS, Zhang H, Xu KZ, et al. 2015. Effects of titanium dioxide nanoparticles on the synthesis of fibroin in silkworm (Bombyx mori). Biological Trace Element Research, 166(2): 225−235. doi: 10.1007/s12011-015-0258-y
    Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33(3): 290−295. doi: 10.1038/nbt.3122
    Qin L, Xia HC, Shi HF, Zhou YJ, Chen L, Yao Q, et al. 2012. Comparative proteomic analysis reveals that caspase-1 and serine protease may be involved in silkworm resistance to Bombyx mori nuclear polyhedrosis virus. Journal of Proteomics, 75(12): 3630−3638. doi: 10.1016/j.jprot.2012.04.015
    Rockenbach MF, Corrêa CCG, Heringer AS, Freitas ILJ, Santa-Catarina C, Do Amaral-Júnior AT, et al. 2018. Differentially abundant proteins associated with heterosis in the primary roots of popcorn. PLoS One, 13(5): e0197114. doi: 10.1371/journal.pone.0197114
    Saeed A, Hoogerland JA, Wessel H, Heegsma J, Derks TGJ, Van Der Veer E, et al. 2020. Glycogen storage disease type 1a is associated with disturbed vitamin A metabolism and elevated serum retinol levels. Human Molecular Genetics, 29(2): 264−273. doi: 10.1093/hmg/ddz283
    Samami R, Seidavi A, Eila N, Moarefi M, Ziaja DJ, Lis JA, et al. 2019. Production performance and economic traits of silkworms (Bombyx mori L., 1758) fed with mulberry tree leaves (Morus alba, var. Ichinose) significantly differ according to hybrid lines. Livestock Science, 226: 133−137. doi: 10.1016/j.livsci.2019.06.015
    Shao L, Xing F, Xu CH, Zhang QH, Che J, Wang XM, et al. 2019. Patterns of genome-wide allele-specific expression in hybrid rice and the implications on the genetic basis of heterosis. Proceedings of the National Academy of Sciences of the United States of America, 116(12): 5653−5658. doi: 10.1073/pnas.1820513116
    Sharma K, Bali K. 2019. Analysis of heterosis in some bivoltine silkworm hybrids of Bombyx mori L. Journal of Entomology and Zoology Studies, 7(5): 1−8.
    Shull GH. 1948. What is "heterosis"?. Genetics, 33(5): 439−446. doi: 10.1093/genetics/33.5.439
    Singer MA, Hortsch M, Goodman CS, Bentley D. 1992. Annulin, a protein expressed at limb segment boundaries in the grasshopper embryo, is homologous to protein cross-linking transglutaminases. Developmental Biology, 154(1): 143−159. doi: 10.1016/0012-1606(92)90055-L
    Singh T, Saratchandra B, Murthy GN. 2002. An analysis of heterosis in the silkworm, Bombyx mori (L. ). International Journal of Industrial Entomology, 5(1): 23−32.
    Springer NM, Stupar RM. 2007. Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. The Plant Cell, 19(8): 2391−2402. doi: 10.1105/tpc.107.052258
    Wang H, Fang Y, Wang LP, Zhu WJ, Ji HP, Wang HY, et al. 2015. Heterosis and differential gene expression in hybrids and parents in Bombyx mori by digital gene expression profiling. Scientific Reports, 5(1): 8750. doi: 10.1038/srep08750
    Wang SH, You ZY, Feng M, Che JQ, Zhang YY, Qian QJ, et al. 2016. Analyses of the molecular mechanisms associated with silk production in silkworm by iTRAQ-based proteomics and RNA-sequencing-based transcriptomics. Journal of Proteome Research, 15(1): 15−28. doi: 10.1021/acs.jproteome.5b00821
    Wang SH, You ZY, Ye LP, Che JQ, Qian QJ, Nanjo Y, et al. 2014. Quantitative proteomic and transcriptomic analyses of molecular mechanisms associated with low silk production in silkworm Bombyx mori. Journal of Proteome Research, 13(2): 735−751. doi: 10.1021/pr4008333
    Wang Y, Gao S, Zhao Y, Chen WH, Shao JJ, Wang NN, et al. 2019. Allele-specific expression and alternative splicing in horse× donkey and cattle× yak hybrids. Zoological Research, 40(4): 293−305. doi: 10.24272/j.issn.2095-8137.2019.042
    Wu XL, Liu Y, Zhang YW, Gu R. 2021. Advances in Research on the Mechanism of Heterosis in Plants. Frontiers in Plant Science, 12: 745726. doi: 10.3389/fpls.2021.745726
    Xiang H, Li X, Dai FY, Xu X, Tan AJ, Chen L, et al. 2013. Comparative methylomics between domesticated and wild silkworms implies possible epigenetic influences on silkworm domestication. BMC Genomics, 14(1): 646. doi: 10.1186/1471-2164-14-646
    Xiang H, Liu XJ, Li MW, Zhu YN, Wang LZ, Cui Y, et al. 2018. The evolutionary road from wild moth to domestic silkworm. Nature Ecology & Evolution, 2(8): 1268−1279.
    Xiang H, Zhu JD, Chen Q, Dai FY, Li X, Li MW, et al. 2010. Single base–resolution methylome of the silkworm reveals a sparse epigenomic map. Nature Biotechnology, 28(5): 516−520. doi: 10.1038/nbt.1626
    Xiao R, Yuan Y, Zhu FF, He SQ, Ge Q, Wang XQ, et al. 2020. Transcriptomics and proteomics-based analysis of heterosis on main economic traits of silkworm. Bombyx mori. Journal of Proteomics, 229: 103941.
    Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, et al. 1997. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proceedings of the National Academy of Sciences of the United States of America, 94(17): 9226−9231. doi: 10.1073/pnas.94.17.9226
    Zhang Y, Tang H, Yang Y, Lü P, Yao Q, Chen K. 2018. Comparative proteomic analysis of the silkworm (Bombyx mori L. ) silk gland reveals yield heterosis. ISJ-Invertebrate Survival Journal, 15(1): 66−82.
    Zhou SR, Xing MQ, Zhao ZL, Gu YC, Xiao YP, Liu QQ, et al. 2021. DNA methylation modification in heterosis initiation through analyzing rice hybrid contemporary seeds. The Crop Journal, 9(5): 1179−1190. doi: 10.1016/j.cj.2020.12.003
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索


    Article Metrics

    Article views (222) PDF downloads(30) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint