Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-22T18:15:01.141Z Has data issue: false hasContentIssue false
  • English
  • Français

Universal and differential transcriptional regulatory pathways involved in the preparation of summer and winter diapauses in Pieris melete

Published online by Cambridge University Press:  01 February 2021

Ting Jiang ,
Yulin Zhu ,
Yingchuan Peng ,
Wanna Zhang  and
Haijun Xiao Open the ORCID record for Haijun Xiao [Opens in a new window]
Ting Jiang
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang330045, China
Yulin Zhu
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang330045, China
Yingchuan Peng
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang330045, China
Wanna Zhang
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang330045, China
Haijun Xiao*
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang330045, China
*
Author for correspondence: Haijun Xiao, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Much progress has been made in understanding the environmental and hormonal systems regulating winter diapause. However, transcriptional regulation of summer diapause is still largely unknown, making it difficult to understand an all-around regulation profile of seasonal adaptation. To bridge this gap, comparison RNA-seq to profile the transcriptome and to examine differential gene expression profiles between non-diapause, summer diapause, and winter diapause groups were performed. A total number of 113 million reads were generated and assembled into 79,117 unigenes, with 37,492 unigenes categorized into 58 functional gene ontology groups, 25 clusters of orthologous group categories, and 256 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. KEGG analysis mapped 2108 differentially expressed genes to 48 and 67 pathways for summer and winter diapauses, respectively. Enrichment statistics showed that 11 identical pathways similarly overlapped in the top 20 enriched functional groups both related to summer and winter diapauses. We also identified 35 key candidate genes for universal and differential functions related to summer and winter diapause preparation. Furthermore, we identified some genes involved in the signaling and metabolic pathways that may be the key drivers to integrate environmental signals into the summer and winter diapause preparation. The current study provided valuable insights into global molecular mechanisms underpinning diapause preparation.

Keywords

Comparative transcriptome analysisdiapause preparationdifferential expressionPieris meletesignal and metabolism pathway
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 3 , June 2021 , pp. 371 - 378
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bao, B and Xu, W (2011) Identification of gene expression changes associated with the initiation of diapause in the brain of the cotton bollworm, Helicoverpa armigera. BMC Genomics 12, 224.CrossRefGoogle ScholarPubMed
Benoit, J (2010) Water management by dormant insects: comparisons between dehydration resistance during summer aestivation and winter diapause. In Arturo Navas, C and Carvalho, JE (eds), Aestivation. Berlin Heidelberg: Springer, pp. 209–229.CrossRefGoogle ScholarPubMed
Deng, Y, Li, F, Rieske, LK, Sun, LL and Sun, SH (2018) Transcriptome sequencing for identification of diapause-associated genes in fall webworm, Hyphantria cunea Drury. Gene 668, 229–236.CrossRefGoogle ScholarPubMed
Dong, Y, Desneux, N, Lei, C and Niu, C (2014) Transcriptome characterization analysis of Bactrocera minax and new insights into its pupal diapause development with gene expression analysis. International Journal of Biological Science 10, 1051–1063.CrossRefGoogle ScholarPubMed
Durant, DR, Berens, AJ, Toth, AL and Rehan, SM (2016) Transcriptional profiling of overwintering gene expression in the small carpenter bee, Ceratina calcarata. Apidologie 47, 572–582.CrossRefGoogle Scholar
Emerson, KJ, Bradshaw, WE and Holzapfel, CM (2010) Microarrays reveal early transcriptional events during the termination of larval diapause in natural populations of the mosquito, Wyeomyia smithii. PLoS ONE 5, e9574.CrossRefGoogle ScholarPubMed
Gong, ZJ, Wu, YQ, Miao, J, Duan, Y, Jiang, YL and Li, T (2013) Global transcriptome analysis of orange wheat blossom midge, Sitodiplosis mosellana (Gehin) (Diptera: Cecidomyiidae) to identify candidate transcripts regulating diapause. PLoS ONE 8, e71564.CrossRefGoogle ScholarPubMed
Goto, M, Li, Y, Kayaba, S, Outani, S and Koichi, S (2001) Cold hardiness in summer and winter diapause and post-diapause pupae of the cabbage armyworm, Mamestra brassicae L. under temperature acclimation. Journal of Insect Physiology 47, 709–714.CrossRefGoogle Scholar
Grabherr, MG, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q, Chen, Z, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, di Palma, F, Birren, BW, Nusbaum, C, Lindblad-Toh, K, Friedman, N and Regev, A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644–652.CrossRefGoogle ScholarPubMed
Hand, SC, Denlinger, DL, Podrabsky, JE and Roy, R (2016) Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 310, 1193–1211.CrossRefGoogle ScholarPubMed
Hao, YJ, Zhang, YJ, Si, FL, Fu, DY, He, ZB and Chen, B (2016) Insight into the possible mechanism of the summer diapause of Delia antiqua (Diptera: Anthomyiidae) through digital gene expression analysis. Insect Science 23, 438–451.CrossRefGoogle ScholarPubMed
Hase, H, Koukai, M, Hamanaka, Y, Goto, SG, Tachibana, S-I and Shiga, S (2017) Transcriptome analysis of the brain under diapause and nondiapause conditions in the blowfly Protophormia terraenovae. Physiological Entomology 42, 282–289.CrossRefGoogle Scholar
Hickner, P, Mori, A, Zeng, E, Tan, J and Severson, D (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, 439–447.CrossRefGoogle ScholarPubMed
Ishikawa, Y, Yamashita, T and Nomura, M (2000) Characteristics of summer diapause in the onion maggot, Delia antiqua (Diptera : Anthomyiidae). Journal of Insect Physiology 46, 161–167.CrossRefGoogle Scholar
King, AM and MacRae, TH (2015) Insect heat shock proteins during stress and diapause. Annual Review of Entomology 60, 59–75.CrossRefGoogle ScholarPubMed
Koštál, V (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Koštál, V and Denlinger, DL (2011) Dormancy and developmental arrest in invertebrates. Journal of Insect Physiology 57, 537.CrossRefGoogle ScholarPubMed
Koštál, V, Štětina, T, Poupardin, R, Korbelová, J and Bruce, AW (2017) Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. Proceedings of the National Academy of Sciences 114, 8532–8537.CrossRefGoogle ScholarPubMed
Kučerová, L, Kubrak, OI, Bengtsson, JM, Strnad, H, Nylin, S, Theopold, U and Nässel, DR (2016) Slowed aging during reproductive dormancy is reflected in genome-wide transcriptome changes in Drosophila melanogaster. BMC Genomics 17, 50.CrossRefGoogle ScholarPubMed
Leal, L, Talla, V, Källman, T, Friberg, M, Wiklund, C, Dincă, V, Vila, R and Backström, N (2018) Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation. Molecular Ecology 27, 935–948.CrossRefGoogle ScholarPubMed
Poelchau, MF, Reynolds, JA, Denlinger, DL, Elsik, CG and Armbruster, PA (2011) A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation. BMC Genomics 12, 619.CrossRefGoogle Scholar
Poelchau, MF, Reynolds, JA, Elsik, CG, Denlinger, DL and Armbruster, PA (2013 a) Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proceedings of the Royal Society B. Biological Sciences 280, 20130143.CrossRefGoogle ScholarPubMed
Poelchau, MF, Reynolds, JA, Elsik, CG, Denlinger, DL and Armbruster, PA (2013 b) RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito, Aedes albopictus. Journal of Experimental Biology 216, 4082–4090.Google ScholarPubMed
Ragland, GJ, Egan, SP, Feder, JL, Berlocher, SH and Hahn, DA (2011) Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. Journal of Experimental Biology 214, 3948–3959.CrossRefGoogle ScholarPubMed
Santos, PKF, de Souza Araujo, N, Francoso, E, Zuntini, AR and Arias, MC (2018) Diapause in a tropical oil-collecting bee: molecular basis unveiled by RNA-Seq. BMC Genomics 19, 305.CrossRefGoogle Scholar
Sim, C and Denlinger, DL (2008) Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proceedings of the National Academy of Sciences 105, 6777–6781.CrossRefGoogle ScholarPubMed
Sim, C and Denlinger, DL (2013) Insulin signaling and the regulation of insect diapause. Frontiers in Physiology 4, 189.CrossRefGoogle ScholarPubMed
Sim, C, Kang, DS, Kim, S, Bai, X and Denlinger, DL (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 112, 3811–3816.CrossRefGoogle ScholarPubMed
Spieth, HR, Xue, F and Strau, K (2004) Induction and inhibition of diapause by the same photoperiod: experimental evidence for a ‘double circadian oscillator clock’. Journal of Biological Rhythms 19, 483–492.CrossRefGoogle Scholar
Tu, XB, Wang, J, Hao, K, Whitman, DW, Fan, YL, Cao, GC and Zhang, ZH (2015) Transcriptomic and proteomic analysis of pre-diapause and non-diapause eggs of migratory locust, Locusta migratoria L. (Orthoptera: Acridoidea). Scientific Report 5, e11402.CrossRefGoogle Scholar
Wang, XP, Ge, F, Xue, FS and You, LS (2004) Diapause induction and clock mechanism in the cabbage beetle, Colaphellus bowringi (Coleoptera: Chrysomelidae). Journal of Insect Physiology 50, 373–381.CrossRefGoogle Scholar
Wu, YK, Zou, C, Fu, DM, Zhang, WN and Xiao, HJ (2018) Molecular characterization of three Hsp90 from Pieris and expression patterns in response to cold and thermal stress in summer and winter diapause of Pieris melete. Insect Science 25, 273–283.CrossRefGoogle Scholar
Xiao, HJ, Yang, D and Xue, FS (2006) Effect of photoperiod on the duration of summer and winter diapause in the cabbage butterfly, Pieris melete (Lepidoptera : Pieridae). European Journal of Entomology 103, 537–540.CrossRefGoogle Scholar
Xiao, HJ, Li, F, Wei, XT and Xue, FS (2008) A comparison of photoperiodic control of diapause between aestivation and hibernation in the cabbage butterfly Pieris melete. Journal of Insect Physiology 54, 755–764.CrossRefGoogle ScholarPubMed
Xiao, HJ, Wu, XF, Wang, Y, Zhu, XF and Xue, FS (2009) Diapause induction and clock mechanism in the cabbage butterfly Pieris melete Ménétriés. Journal of Insect Physiology 55, 488–493.CrossRefGoogle ScholarPubMed
Xiao, HJ, Wu, SH, He, HM, Chen, C and Xue, FS (2012) Role of natural day-length and temperature in determination of summer and winter diapause in Pieris melete (Lepidoptera: Pieridae). Bulletin of Entomological Research 102, 267–273.CrossRefGoogle Scholar
Xiao, HJ, W, SH, Chen, C and Xue, FS (2013) Optimal low temperature and chilling period for both summer and winter diapause development in Pieris melete: based on a similar mechanism. PLoS ONE 8, e56404.CrossRefGoogle Scholar
Xu, W, Lu, Y and Denlinger, D (2012) Cross-talk between the fat body and brain regulates insect developmental arrest. Proceedings of the National Academy of Sciences 109, 14687–14692.CrossRefGoogle ScholarPubMed
Yocum, GD, Rinehart, JP, Horvath, DP, Kemp, WP, Bosch, J, Alroobi, R and Salem, S (2015) Key molecular processes of the diapause to post-diapause quiescence transition in the alfalfa leafcutting bee Megachile rotundata identified by comparative transcriptome analysis. Physiological Entomology 40, 103–112.CrossRefGoogle Scholar
Zhai, Y, Dong, X, Gao, H, Chen, H, Yang, P, Li, P, Yin, Z, Zheng, L and Yu, Y (2019) Quantitative proteomic and transcriptomic analyses of metabolic regulation of adult reproductive diapause in Drosophila suzukii (Diptera: Drosophilidae) females. Frontiers in Physiology 10, 344.CrossRefGoogle ScholarPubMed
Zhang, Q, Nachman, RJ, Kaczmarek, K, Zabrocki, J and Denlinger, DL (2011) Disruption of insect diapause using agonists and an antagonist of diapause hormone. Proceedings of the National Academy of Sciences 108, 16922–16926.CrossRefGoogle Scholar
Zhao, JY, Zhao, XT, Sun, JT, Zou, LF, Yang, SX, Han, X, Zhu, WC, Yin, Q and Hong, XY (2017) Transcriptome and proteome analyses reveal complex mechanisms of reproductive diapause in the two-spotted spider mite, Tetranychus urticae. Insect Molecular Biology 26, 215–232.CrossRefGoogle ScholarPubMed
Supplementary material: File

Jiang et al. supplementary material

Jiang et al. supplementary material

Download Jiang et al. supplementary material(File)
File 2.2 MB