Transcriptomic and proteomic analysis of Locusta migratoria eggs at different embryonic stages: Comparison for diapause and non-diapause regimes

doi:10.1016/S2095-3119(16)61529-0

摘要/Abstract

Abstract: Temperate-zone insects typically survive winter by entering diapause. Although many aspects of insect diapause have been studied, the underlying molecular mechanism of insect diapause is not well understood. Here we report the results of the transcriptional and translational differences of migratory locust eggs at different embryonic states using diapause (low temperature) and non-diapause (high temperature) regimes. Compared with non-diapause eggs at 100 degree-days (N2) treatment, 29 671 transcripts and 296 proteins were differentially expressed at the diapause maintenance stage (D2).While compared with 150 degree-days (N3) treatment, 45 922 transcripts and 404 proteins were differentially expressed in the post-diapause stage (D3). Among them, 51 and 102 transcripts had concurrent transcription and translation profiles in D2 vs. N2 and D3 vs. N3 treatments, respectively. Analysis of Gene Ontology categorized these genes and proteins into three categories: biological processes, cellular components, and molecular functions. Biological pathway analysis indicated that three pathways: (1) insect hormone biosynthesis (KEGG: Map 00981), (2) the insulin signaling pathway (KEGG: Map 04910), and (3) the peroxisome proliferator-activated receptor (PPAR) signaling pathway (KEGG: Map 03320) play an important role in locust diapause regulation. Most of these transcripts and proteins were up-regulated in the diapause treatments, and were highly linked to juvenile hormone biosynthesis, insulin and PPAR signaling pathways, suggesting these three pathways may be involved in diapause and development regulation. This study demonstrates the applicability of high-throughput omics tools to identify biochemical pathways linked to diapause in locust egg development. In addition, it reveals that cellular metabolism in diapause eggs is more inactive than in non-diapause eggs, and most of the down-regulated enzymes and pathways are related to reduce energy loss.

Key words: Locusta migratoria , diapause , transcriptome , proteome , molecular mechanism

. [J]. Journal of Integrative Agriculture, 2017, 16(08): 1777-1788.

HAO Kun, WANG Jie, TU Xiong-bing, Douglas W. Whitman, ZHANG Ze-hua. Transcriptomic and proteomic analysis of Locusta migratoria eggs at different embryonic stages: Comparison for diapause and non-diapause regimes[J]. Journal of Integrative Agriculture, 2017, 16(08): 1777-1788.

参考文献

Agre P. 2006. The aquaporin water channels. Proceedings of the American Thoracic Society, 3, 5–13.

Ahmad S A, Hopkins T L. 1993. β-Glucosylation of plant phenolics by phenol β-glucosyltransferase in larval tissues of the tobacco hornworm, Manduca sexta (L.). Insect Biochemstry and Molecular Biology, 23, 581–589.

Ando Y. 1972. Egg diapause and water absorption in the false melon beetle, Atrachya menetriesi Faldermann (Coleoptera: Chrysomelidae). Applied Entomology and Zoology, 7, 142–154.

Bryon A, Wybouw N, Dermauw W, Tirry L, Van Leeuwen T. 2013. Genome wide gene-expression analysis of facultative reproductive diapause in the two-spotted spider mite Tetranychus urticae. BMC Genomics, 14, 1–20.

Carolan J C, Caragea D, Reardon K T, Mutti N S, Dittmer N, Pappan K, Cui F, Castaneto M, Poulain J, Dossat C. 2011. Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): A dual transcriptomic/proteomic approach. Journal of Proteome Research, 10, 1505–1518.

Chen Y L. 2007. The Main Locust and Ecological Management of Locust Plague in China. Science Press, Beijing. (in Chinese)

Colinet H, Renault D, Charoy-Guével B, Com E. 2012. Metabolic and proteomic profiling of diapause in the aphid parasitoid Praon volucre. PLOS ONE, 7, e32606.

Conesa A, Götz S, García-Gómez J M, Terol J, Talón M, Robles M. 2005. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674–3676.

Cunha I, Galante-Oliveira S, Rocha E, Planas M, Urbatzka R, Castro L. 2013. Dynamics of PPARs, fatty acid metabolism genes and lipid classes in eggs and early larvae of a teleost. Comparative Biochemistry and Physiology (Part B: Biochemistry and Molecular Biology), 164, 247–258.

Denlinger D L. 2002. Regulation of diapause. Annual Review of Entomology, 47, 93–122.

Denlinger D L, Yocum G D, Rinehart J P. 2005. Hormonal control of diapause. Comprehensive Molecular Insect Science, 3, 615–650.

Guo F, Chen Y L, Lu B L. 1991. The Biology of the Migratory Locusts in China. Shandong Science and Technology Press, Shandong. (in Chinese)

Hakomori T, Tanaka S. 1992. Genetic control of diapause and other developmental traits in Japanese strains of the migratory locust, Locusta migratoria L.: univoltine vs. bivoltine. Japan Journal of Entomology, 60, 319–328.

Hickner P V, Mori A, Zeng E, Tan J C, Severson D W. 2015. Whole transcriptome responses among females of the filariasis and arbovirus vector mosquito Culex pipiens implicate TGF-β signaling and chromatin modification as key drivers of diapause induction. Functional & Integrative Genomics, 15, 1–9.

Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T. 2008. KEGG for linking genomes to life and the environment. Nucleic Acids Research, 36, 480–484.

Kankare M, Salminen T, Laiho A, Vesala L, Hoikkala A. 2010. Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: A candidate gene microarray study. BMC Ecology, 10, 1–9.

Kislinger T, Cox B, Kannan A, Chung C, Hu P, Ignatchenko A, Scott M S, Gramolini A O, Morris Q, Hallett M T. 2006. Global survey of organ and organelle protein expression in mouse: Combined proteomic and transcriptomic profiling. Cell, 125, 173–186.

Kostál V. 2006. Eco-physiological phases of insect diapause. Journal of Insect Physiology, 52, 113–127.

Krysan J L, Jackson J J, Lew A C. 1984. Field termination of egg diapause in diabrotica with new evidence of extended diapause in D. barberi (Coleoptera: Chrysomelidae). Environmental Entomology, 13, 1237–1240.

Küppers E, Gleiser C, Brito V, Wachter B, Pauly T, Hirt B, Grissmer S. 2008. AQP4 expression in striatal primary cultures is regulated by dopamine-implications for proliferation of astrocytes. European Journal of Neuroscience, 28, 2173–2182.

Langdon C M, MacRae T H. 1989. The diversity of α-tubulin during artemia prelarval development. Cell and Molecular Biology of Artemia Development, 174, doi: 10.1007/978-1-4757-0004-6_43

Liu M J, Tong X L, Zhang G J. 2014. Advance in researches of the mechanism of diapause in the silkworm, Bombyx mori. Newsletter of Sericultural Science, 34, 23–32. (in Chinese)

Lu M, Cao S, Du Y, Liu Z, Liu P, Li J. 2013. Diapause, signal and molecular characteristics of overwintering Chilo suppressalis (Lepidoptera: Pyralidae). Scientific Reports, 3, 3211.

Lu X, Li J, Yang J, Liu X, Ma J. 2014. De novo transcriptome of the desert beetle Microdera punctipennis (Coleoptera: Tenebrionidae) using illumina RNA-seq technology. Molecular Biology Reports, 41, 7293–7303.

Marcus N H. 1987. Differences in the duration of egg diapause of Labidocera aestiva (Copepoda: Calanoida) from the Woods Hole, Massachusetts region. Biological Bulletin, 173, 169–177.

Müller E M, Hub J S, Grubmüller H, de Groot B L. 2008. Is TEA an inhibitor for human aquaporin-1? Pflügers Archiv-

European Journal of Physiology, 456, 663–669.

Parrotta L, Cai G, Cresti M. 2010. Changes in the accumulation of α-and β-tubulin during bud development in Vitis vinifera L. Planta, 231, 277–291.

Poelchau M F, Reynolds J A, Denlinger D L, Elsik C G, Armbruster P A. 2011. A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation. BMC Genomics, 12, 251–254.

Ponnuvel K M, Sasibhushan S, Geetha N M, Rao C. 2015. Diapause-related gene expression in eggs of multivoltine Bombyx mori L. silk worm races. In: New Horizons in Insect Science: Towards Sustainable Pest Management. Springer Press, India.

Price D R G, Karley A J, Ashford D A, Isaacs H V, Pownall M E, Wilkinson H S, Gatehouse J A, Douglas A E. 2007. Molecular characterization of a candidate gut sucrase in the pea aphid Acyrthosiphon pisum. Insect Biochemistry and Molecular Biology, 37, 307–317.

Randall D D, Derr R F. 1965. Trehalose: occurrence and relation to egg diapause and active transport in the differential grasshopper, Melanoplus differentialis. Journal of Insect Physiology, 11, 329–335.

Saavedra M, Masdeu M, Hale P, Sibbons C M, Holt W V. 2014. Dietary fatty acid enrichment increases egg size and quality of yellow seahorse Hippocampus kuda. Animal Reproduction Science, 145, 54–61.

Sasibhushan S, Rao C, Ponnuvel K M. 2013. Genome wide microarray based expression profiles during early embryogenesis in diapause induced and non-diapause eggs of polyvoltine silkworm Bombyx mori. Genomics, 102, 379–387.

Sim C, Denlinger D L. 2013. Insulin signaling and the regulation of insect diapause. Frontiers in Physiology, 4, 189.

Sim C, Kang D S, Kim S, Bai X, Denlinger D L. 2015. Identification of FOXO targets that generate diverse features of the diapause phenotype in the mosquito Culex pipiens. Proceedings of the National Academy of Sciences of the United States of America, 112, 3811–3816.

Sinha A, Sommer R J, Dieterich C. 2012. Divergent gene expression in the conserved dauer stage of the nematodes Pristionchus pacificus and Caenorhabditis elegans. BMC Genomics, 13, 254.

Song J, Sun R, Li D, Tan F, Li X, Jiang P, Huang X, Lin L, Deng Z, Zhang Y. 2012. An improvement of shotgun proteomics analysis by adding next-generation sequencing transcriptome data in orange. PLOS ONE, 7, e39494.

Sota T, Mogi M.1992. Survival time and resistance to desiccation of diapause and non-diapause eggs of temperate Aedes (Stegomyia) mosquitoes. Entomologia Experimentalis et Applicata, 63, 155–161.

Stuckas H, Mende M B, Hundsdoerfer A K. 2014. Response to cold acclimation in diapause pupae of Hyles euphorbiae (Lepidoptera: Sphingidae): Candidate biomarker identification using proteomics. Insect Molecular Biology, 23, 444–456.

Tanaka H. 1994. Embryonic diapause and life cycle in the migratory locust, Locusta migratoria L. (Orthoptera: Acrididae), in Kyoto. Applied Entomology and Zoology, 29, 179–191.

Tanaka S. 1992. The significance of embryonic diapause in a Japanese strain of the migratory locust, Locusta migratoria (Orthoptera, Acrididae). Japan Journal of Entomology, 60, 503–520.

Tanaka S, Zhu D H. 2008. Geographic variation in embryonic diapause, cold-hardiness and life cycles in the migratory locust Locusta migratoria (Orthoptera: Acrididae) in China. Entomological Science, 11, 327–339.

Tu X, Wang J, Hao K, Whitman D W, Fan Y, Cao G, Zhang Z. 2015. Transcriptomic and proteomic analysis of pre-diapause and non-diapause eggs of migratory locust, Locusta migratoria L. (Orthoptera: Acridoidea). Scientific Reports, 5, 11402.

Uvarov B P. 1966. Grasshoppers and Locusts. vol. 1. Cambridge University Press, London.

Uvarov B P. 1977. Grasshoppers and Locusts. vol. 2. Cambridge University Press, London.

Wang Q, Hasan G, Pikielny C W. 1999. Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster, the antennae. The Journal of Biological Chemistry, 274, 10309–10315.

Whitman D W, Ananthakrishnan T N. 2009. Phenotypic Plasticity of Insects: Mechanisms and Consequences. CRC Press, Florida.

Yu S J. 1989. β-Glucosidase in four phytophagous Lepidoptera. Insect Biochemistry, 19, 103–108.