Current Science

Open Access Open Access  Restricted Access Subscription Access

A transcriptomic approach reveals the molecular basis of pre-pupal diapause of Red Banded Mango Caterpillar, Deanolis sublimbalis


Affiliations
1 College of Horticulture, Dr Y. S. R. Horticultural University, Venkataramannagudem 534 101, India
2 Division of Crop Protection, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
 

The Red Banded Mango Caterpillar (RBMC), Deanolis sublimbalis Snellen (Lepidoptera: Crambidae), a devastating monophagous pest of mango (Mangifera indica L.), enters a pre-pupal diapause in the absence of host fruits synchronizing its life cycle with seasonal fruiting across southeast Asia and Oceania. Considering its unique nature, a detailed de novo transcriptome analysis was carried out on different physiological stages of RBMC pupae to understand the mechanisms underlying diapause. A total of 102 differentially expressed unigenes were identified with altered expression patterns (55 upregulated and 47 downregulated) and consequently mapped to various pathways associated with diapause. Three major pathways, i.e. proteasome, Epstein–Barr virus infection and lipoic acid metabolism were significantly (P < 0.01) enriched during the diapause phase in D. sublimbalis. From the three pathways, 16 differentially expressed genes (15 up-regulated and 1 down-regulated) were identified to play a vital role in diapause management. To our knowledge, no earlier studies have identified diapause-related genes in D. sublimbalis. The information gained from the present study can be exploited to develop control strategies involving molecular tools.
User
Notifications
Font Size

  • Denlinger, D. L., Regulation of diapause. Annu. Rev. Entomol., 2002, 47, 93–122.

  • MacRae, T. H., Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci., 2010, 67, 2405–2424.

  • Liu, J. Y. and Lin, J. R., Diapause induction and termination of Bombyx mori. Guangdong Canye, 2011, 45, 35–38.

  • Kostal, V., Eco-physiological phases of insect diapause. J. Insect Physiol., 2006, 52, 113–127.

  • Senguptha, G. C. and Behura, B. K., Some new records of crop pests from India. Indian J. Entomol., 1955, 17, 283–285.

  • Tipon, H. T., Seed borer in mango. In Paper present at the Second National Fruit Crop Symposium, Cebu City, Philippines, 12–14 December 1979.

  • Kalshoven, L. G. E., The Pests of Crops in Indonesia, PT Ichtiar Baru – Van Hoeve Jakarta, Indowara, 1981, p. 701.

  • Golez, H. G., Bionomics and control of mango seed borer Noorda albizonalis Hampson (Pyralidae: Lepidoptera). Acta Hortic., 1991, 291, 418–424.

  • Jha, S. and Sarkar, A., Mango in Malda, Bidhan Chandra Krishi Viswavidyalaya, Noida, 1991, p. 13.

  • Zaheruddeen, S. M. and Sujatha, A., Record of Deanolis albizonalis (Hampson.) (Pyralidae: Odontinae) as mango fruit borer in Andhra Pradesh. J. Bombay Natl. Hist. Soc., 1993, 90, 528.

  • Waterhouse, D. F., Biological Control of Insect Pest: Southeast Asian Prospects, ACIAR Monograph, 1998, vol. 5, p. 548.

  • Krull, S. M. E., Studies on the mango-ecosystem in Papua New Guinea with special reference to the ecology of Deanolis sublimbalis Snellen (Lepidoptera, Pyralidae) and to the biological control of Ceroplastes rubens (Homoptera, Coccidae). Ph D thesis, Justus-Liebig-Universitat Gieben, Germany, 2004, p. 190.

  • Pinese, B., Biology, damage levels and control of red-banded mango caterpillar in Papua New Guinea and Australia – project update. Australian Centre for International Agricultural Research (on-line), 2005; http://www.aciar.gov.au/web.nsf/doc/ACIA-68K3JQ (accessed on 11 January 2006).

  • Tenakanai, D., Dori, F. and Kurika, K., Red-banded mango caterpillar, Deanolis sublimbalis Snellen. (Lepidoptera: Pyralidae: Odontinae), in Papua New Guinea. In Pest and Disease Incursions: Risks, Threats and Management in Papua New Guinea, ACIAR Technical Reports, 2006, no. 62, pp. 161–165.

  • Fenner, T., Red-banded mango caterpillar: biology and control prospects. Northern Territory Department of Primary Industry and Fisheries, Queensland, 1997, p. 2.

  • Poelchau, M. F., Reynolds, J. A., Denlinger, D. L., Elsik, C. G., Armbruster, P. A. and Denovo, A., Transcriptome of the Asian tiger mosquito, Aedes albopictus to identify candidate transcripts for diapause preparation. BMC Genomics, 2011, 12, 619.

  • Poelchau, M. F., Reynolds, J. A., Denlinger, D. L., Elsik, C. G. and Armbruster, P. A., Transcriptome sequencing as a platform to elucidate molecular components of the diapause response in the Asian tiger mosquito Aedes albopictus. Physiol. Entomol., 2013, 38, 173–181.

  • Poelchau, M. F., Reynolds, J. A., Elsik, C. G., Denlinger, D. L. and Armbruster, P. A., Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. London, Ser. B, 2013, 280, 20130–20143.

  • Dong, Y., Desneux, N., Lei, C. and Niu, C., Transcriptome characterization analysis of Bactrocera minax and new insights into its pupal diapause development with gene expression analysis. Int. J. Biol. Sci., 2014, 10, 1051–1063.

  • Cheolho, S. and Denlinger, D. L., Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl. Acad. Sci. USA, 2008, 105, 6777–6781.

  • Fukuda, S. and Takeuchi, S., Diapause factor-producing cells in the suboesophageal ganglion of the silkworm, Bombyx mori L. Proc. Jpn. Acad., 1967, 43, 51–56.

  • Fukuda, S. and Takeuchi, S., Studies on the diapause factors producing cells in the suboesophageal ganglion of the silkworm, Bombyx mori L. Embryologia, 1967, 4, 333–353.

  • Imai, K., Konno, T., Nakazawa, Y., Komiya, T., Isobe, M. and Koga, K., Isolation and structure of diapause hormone of the silkworm, Bombyx mori. Proc. Jpn. Acad. Ser. B, 1991, 67, 98–101.

  • Kankare, M., Parker, D., Merisalo, M., Salminen, T. S. and Hoikkala, A., Transcriptional differences between diapausing and non-diapausing D. montana females reared under the same photoperiod and temperature. PLoS ONE, 2016, 11, 0161852.

  • Ewels, P., Magnusson, M., Lundin, S. and Kaller, M., MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 2016, 32, 3047–3048.

  • Bolger, A. M., Lohse, M. and Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 2014, 30, 2114–2120.

  • Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A. and Amit, I., Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol., 2011, 29, 644–652.

  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J. and Bealer, K., BLAST+: architecture and applications. BMC Bioinform., 2009, 10, 421.

  • Ye, J., Fang, L., Zheng, H., Zhang, Y., Chen, J. and Zhang, Z., WEGO: a web tool for plotting GO annotations. Nucleic Acids Res., 2006, 34, 293–297.

  • Langmead, B., Aligning Short Sequencing Reads with Bowtie, Curr. Protoc. Bioinform., 2010, 11, 7; https://doi.org/10.1002/0471250953.bi1107s32.

  • Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J. and Homer, N., The Sequence Alignment/Map format and SAM tools. Bioinformatics, 2009, 25, 2078–2079.

  • Love, M. I., Huber, W. and Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 2014, 15, 550.

  • Maere, S., Heymans, K. and Kuiper, M., BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics, 2005, 21, 3448–3449.

  • Hodek, I., Diapause development, diapause termination and the end of diapause. Eur. J. Entomol., 1996, 93, 475–487.

  • Tauber, M. J. and Tauber, C. A., Insect seasonality: diapause maintenance, termination, and post diapause development. Annu. Rev. Entomol., 1976, 21, 81–107.

  • Tauber, M. J. Tauber, C. A. and Masaki, S., Seasonal Adaptations of Insects, Oxford University Press, NY, USA, 1986.

  • Sujatha, A. and Zaheruddeen, S. M., Biology of Pyralid fruit borer Deanolis albizonalis (Hampson): a new pest of mango. J. Appl. Zool. Res., 2002, 13, 1–5.

  • Fujiwara, K., Suzuki, M., Okumachi, Y., Okamura Ikeda, K., Fujiwara, T., Takahashi, E. I. and Motokawa, Y., Molecular cloning, structural characterization and chromosomal localization of human lipoyl transferase gene. Eur. J. Biochem., 1999, 260, 761–767.

  • Arrese, E. L. and Soulages, J. L., Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol., 2010 55, 207–225; doi:10.1146/annurev-ento-112408-085356.

  • Toprak, U., Hegedus, D., Dogan, C. and Guney, G., A journey into the world of insect lipid metabolism. Arch. Insect Biochem. Physiol., 2020, 104(2), e21682.

  • Bheda, A., Shackelford, J. and Pagano, J. S., Expression and functional studies of ubiquitin C-terminal hydrolase L1 regulated genes. PLoS ONE, 2009, 4, 6764.

  • Li, Y., Zhou, Z., Shen, M., Ge, L. and Liu, F., Ubiquitin-conjugating enzyme E2 E inhibits the accumulation of Rice Stripe virus in Laodelphax striatellus (Fallen). Viruses, 2020, 12, 908.

  • Walters, K. J., Goh, A. M., Wang, Q., Wagner, G. and Howley, P. M., Ubiquitin family proteins and their relationship to the proteasome: a structural perspective. Biochim. Biophys. Acta, 2004, 1695, 73–87.

  • Ikeda, F., Ubiquitin conjugating enzymes in the regulation of the autophagy-dependent degradation pathway. Matrix Biol., 2021, 100–101, 23–29; doi:10.1016/j.matbio.2020.11.004.

  • Donaldson, T. D., Noureddine, M. A., Reynolds, P. J., Bradford, W. and Duronio, R. J., Targeted disruption of Drosophila Roc1b reveals functional differences in the Roc subunit of cullin-dependent E3 ubiquitin ligases. Mol. Biol. Cell, 2004, 15, 4892–4903.

  • Wang, J., Ran, L. L., Li, Y. and Liu, Y. H., Comparative proteomics provides insights into diapause program of Bactrocera minax (Diptera: Tephritidae). PLoS ONE, 2020, 15(12), e0244493.

  • Williams, K. D., Busto, M., Suster, M. L., So, A. K. C., BenShahar, Y. and Leevers, S. J., Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proc. Nat. Acad. Sci. USA, 2006, 103, 15911–15915.

  • Hao, K., Ullah, H., Jarwar, A. R., Nong, X. Q., Tu, X. B. and Zhang, Z. H., Molecular identification and diapause-related functional characterization of a novel dual-specificity kinase gene, MPKL, in Locusta migratoria. FEBS Lett., 2019, 593, 3064–3074.

  • Lin, J. L., Lin, P. L. and Gu, S. H., Phosphorylation of glycogen synthase kinase-3  in relation to diapause processing in the silkworm, Bombyx mori. J. Insect Physiol., 2009, 55, 593–598.

  • Kidokoro, K., Iwata, K., Takeda, M. and Fujiwara, Y., Involvement of ERK/MAPK in regulation of diapause intensity in the false melon beetle, Atrachya menetriesi. J. Insect Physiol., 2006, 52, 1189–1193.

  • Fujiwara, Y. and Shiomi, K., Distinct effects of different temperatures on diapause termination, yolk morphology and MAPK phosphorylation in the silkworm, Bombyx mori. J. Insect Physiol., 2006, 52, 1194–1201.

  • Hao, Y. J., Zhang, Y. J., Si, F. L., Fu, D. Y., He, Z. B. and Chen, B., Insight into the possible mechanism of the summer diapause of Delia antiqua (Diptera: Anthomyiidae) through digital gene expression analysis. Insect Sci., 2016, 23, 438–451.

  • Duan, T. F., Li, L., Tan, Y., Li, Y. Y. and Pang, B. P., Identification and functional analysis of microRNAs in the regulation of summer diapause in Galeruca daurica. Comp. Biochem. Physiol. D, 2020, 100786.

  • Iwata, K. I., Fujiwara, Y. and Takeda, M., Effects of temperature, sorbital, alanine and diapause hormone on embryonic development in Bombyx mori: in vitro tests of old hypothesis. Physiol. Entomol., 2005, 30, 317–323.

  • Fujiwara, Y., Shindome, C., Takeda, M. and Shiomi, K., The roles of ERK and P38 MAPK signaling cascades on embryonic diapause initiation and termination of the silkworm, Bombyx mori. Insect Biochem. Mol. Biol., 2006, 36, 47–53.

  • Kidokoro, K., Iwata, K., Fujiwara, Y. and Takeda, M., Effects of juvenile hormone analogs and 20-hydroxyecdysone on diapause termination in eggs of Locusta migratoria and Oxya yezoensis. J. Insect Physiol., 2006, 52, 473–479.

  • Fujiwara, Y., Tanaka, Y., Iwata, K., Rubio, R. O., Yaginuma, T., Yamashita, O. and Shiomi, K., ERK/MAPK regulates ecdysteroid and sorbitol metabolism for embryonic diapause termination in the silkworm, Bombyx mori. J. Insect Physiol., 2006, 52, 569–575.

  • Fujiwara, Y. and Denlinger, D. L., MAPK is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly Sarcophaga crassipalpis. J. Exp. Biol., 2007, 210, 3295–3300.

  • Cronan, J. E., Progress in the enzymology of the mitochondrial diseases of lipoic acid requiring enzymes. Front. Genet., 2020, 11, 510.

  • Clark, E. W. and Chadbourne, D. S., A comparative study of the weight, lipid, and water content of the pink bollworm. Ann. Entomol. Soc. Am., 1962, 55, 225–228.

  • Hahn, D. A. and Denlinger, D. L., Meeting the energetic demands of insect diapause: nutrient storage and utilization. J. Insect Physiol., 2007, 53, 760–773.

  • Griffin, M. and Sul, H. S., Insulin regulation of fatty acid synthase gene transcription: roles of USF and SREBP-1c. IUBMB Life, 2004, 56, 595–600.

  • Alabaster, A., Isoe, J., Zhou, G., Lee, A., Murphy, A., Day, W. A. and Miesfeld, R. A., Deficiencies in acetyl-CoA carboxylase and fatty acid synthase 1 differentially affect eggshell formation and blood meal digestion in Aedes aegypti. Insect Biochem. Mol. Biol., 2011, 41, 946–955.

  • Majerowicz, D. and Gondim, K. C., Insect Lipid Metabolism: Insights into Gene Expression Regulation. Recent Trends in Gene Expression, Nova Science Publishers, 2013, pp. 147–190.

  • Xue, F., Spieth, H. R., Li, A. and Ai, H., The role of photoperiod and temperature in determination of summer and winter diapause in the cabbage beetle, Colaphellus bowringi (Coleoptera: Chrysomelidae). J. Insect Physiol., 2002, 48, 279–286.

  • Qi, X., Zhang, L., Han, Y., Ren, X., Huang, J. and Chen, H., De novo transcriptome sequencing and analysis of Coccinella septempunctata L. in non-diapause, diapause and diapauses terminated states to identify diapauses associated genes. BMC Genomics, 2015, 16, 1086.


Abstract Views: 244

PDF Views: 121




  • A transcriptomic approach reveals the molecular basis of pre-pupal diapause of Red Banded Mango Caterpillar, Deanolis sublimbalis

Abstract Views: 244  |  PDF Views: 121

Authors

Gandham Krishnarao
College of Horticulture, Dr Y. S. R. Horticultural University, Venkataramannagudem 534 101, India
Avvaru Sujatha
College of Horticulture, Dr Y. S. R. Horticultural University, Venkataramannagudem 534 101, India
Pola Sunitha
College of Horticulture, Dr Y. S. R. Horticultural University, Venkataramannagudem 534 101, India
Meenal Vyas
Division of Crop Protection, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
Pagadala Damodaram Kamala Jayanthi
Division of Crop Protection, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India

Abstract


The Red Banded Mango Caterpillar (RBMC), Deanolis sublimbalis Snellen (Lepidoptera: Crambidae), a devastating monophagous pest of mango (Mangifera indica L.), enters a pre-pupal diapause in the absence of host fruits synchronizing its life cycle with seasonal fruiting across southeast Asia and Oceania. Considering its unique nature, a detailed de novo transcriptome analysis was carried out on different physiological stages of RBMC pupae to understand the mechanisms underlying diapause. A total of 102 differentially expressed unigenes were identified with altered expression patterns (55 upregulated and 47 downregulated) and consequently mapped to various pathways associated with diapause. Three major pathways, i.e. proteasome, Epstein–Barr virus infection and lipoic acid metabolism were significantly (P < 0.01) enriched during the diapause phase in D. sublimbalis. From the three pathways, 16 differentially expressed genes (15 up-regulated and 1 down-regulated) were identified to play a vital role in diapause management. To our knowledge, no earlier studies have identified diapause-related genes in D. sublimbalis. The information gained from the present study can be exploited to develop control strategies involving molecular tools.

References





DOI: https://doi.org/10.18520/cs%2Fv123%2Fi3%2F471-481