Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-08T13:26:28.933Z Has data issue: false hasContentIssue false
  • English
  • Français

Proteins from eggs of the spittlebug Mahanarva spectabilis (Hemiptera: Cercopidae) reveal clues about its diapause regulation

Published online by Cambridge University Press:  27 August 2021

Nayara B. Saraiva ,
Alexander M. Auad ,
Edvaldo Barros ,
Flaviane S. Coutinho ,
Jorge F. Pereira Open the ORCID record for Jorge F. Pereira [Opens in a new window] ,
Rafael A. Barros ,
Humberto J. O. Ramos  and
Maria G. A. Oliveira
Nayara B. Saraiva
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil
Alexander M. Auad
Affiliation:
Embrapa Gado de Leite, CEP 36038-330, Juiz de Fora, MG, Brazil
Edvaldo Barros
Affiliation:
Núcleo de Análise de Biomoléculas, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil
Flaviane S. Coutinho
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil
Jorge F. Pereira*
Affiliation:
Embrapa Gado de Leite, CEP 36038-330, Juiz de Fora, MG, Brazil
Rafael A. Barros
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil
Humberto J. O. Ramos
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil Núcleo de Análise de Biomoléculas, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil
Maria G. A. Oliveira
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil
*
Author for correspondence: Jorge F. Pereira, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Embryo development in eggs of the spittlebug Mahanarva spectabilis (Distant) (Hemiptera: Cercopidae) passes through four phases (known as S1 to S4) being stopped at S2 during diapause. Studies about the molecular basis of diapause in spittlebugs are nonexistent. Here, we analyzed proteins from non-diapausing (ND), diapausing (D) and post-diapausing (PD) eggs of the spittlebug M. spectabilis. In total, we identified 87 proteins where 12 were in common among the developmental and diapause phases and 19 remained as uncharacterized. Non-diapausing eggs (S2ND and S4ND) showed more proteins involved in information storage and processing than the diapausing ones (S2D). Eggs in post-diapausing (S4PD) had a higher number of proteins associated with metabolism than S2D. The network of protein interactions and metabolic processes allowed the identification of different sets of molecular interactions for each developmental and diapause phases. Two heat shock proteins (Hsp65 and Hsp70) along with two proteins associated with intracellular signaling (MAP4K and a serine/threonine-protein phosphatase) were found only in diapausing and/or post-diapausing eggs and are interesting targets to be explored in future experiments. These results shine a light on one key biological process for spittlebug survival and represent the first search for proteins linked to diapause in this important group of insects.

Keywords

EggdiapauseMahanarva spectabilispost-diapausespittlebug
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 2 , April 2022 , pp. 219 - 227
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

Adams, TS, Filipi, PA and Yi, SX (2002) Effect of age, diet, diapause and juvenile hormone on oogenesis and the amount of vitellogenin and vitellin in the two spotted stink bug, Perillus bioculatus (Heteroptera: Pentatomidae). Journal of Insect Physiology 48, 477–486.CrossRefGoogle Scholar
Alvarenga, R, Auad, AM, Moraes, JC, Silva, SEB and Rodrigues, BS (2019) Tolerance to nymphs and adults of Mahanarva spectabilis (Hemiptera: Cercopidae) by forage plants in fertilized soils. Pest Management Science 75, 2242–2250.CrossRefGoogle ScholarPubMed
Assad, ED, Sano, EE, Masutomo, R, Castro, LHR and Silva, FAM (1993) Veranicos na região dos cerrados brasileiros: freqüência e probalidade de ocorrência. Pesquisa Agropecuária Brasileira 28, 993–1003.Google Scholar
Auad, AM and Carvalho, CA (2009) Desenvolvimento e viabilidade de ovos de Mahanarva spectabilis (Distant, 1909) (Hemiptera: Cercopidae) submetidos a diferentes regimes de hidratação. Arquivos do Instituto Biológico 76, 711–714.CrossRefGoogle Scholar
Auad, AM, Simoes, AD, Leite, MV, Silva, SEB, Santos, DR and Monteiro, PH (2011) Seasonal dynamics of egg diapause in Mahanarva spectabilis (Distant, 1909) (Hemiptera: Cercopidae) on elephant grass. Arquivos do Instituto Biológico 78, 325–330.CrossRefGoogle Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Bryon, A, Kurlovs, AH, Van Leeuwen, T and Clark, RM (2017) A molecular-genetic understanding of diapause in spider mites: current knowledge and future directions. Physiological Entomology 42, 211–224.CrossRefGoogle Scholar
Colinet, H, Renault, D, Charoy-Guével, B and Com, E (2012) Metabolic and proteomic profiling of diapause in the aphid parasitoid Praon volucre. PLoS ONE 7, e32606.CrossRefGoogle ScholarPubMed
Cui, DN, Tu, XB, Hao, K, Raza, A, Chen, J, McNeill, M and Zhang, ZH (2019) Identification of diapause-associated proteins in migratory locust, Locusta migratoria L. (Orthoptera: Acridoidea) by label-free quantification analysis. Journal of Integrative Agriculture 18, 2579–2588.CrossRefGoogle Scholar
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 Sciences 10, 1051–1063.CrossRefGoogle ScholarPubMed
Fan, L, Lin, J, Zhong, Y and Liu, J (2013) Shotgun proteomic analysis on the diapause and non-diapause eggs of domesticated silkworm Bombyx mori. PLoS ONE 8, e60386.CrossRefGoogle ScholarPubMed
Fujiwara, Y and Denlinger, DL (2007) High temperature and hexane break pupal diapause in the flesh fly, Sarcophaga crassipalpis, by activating ERK/MAPK. Journal of Insect Physiology 53, 1276–1282.CrossRefGoogle ScholarPubMed
Fujiwara, Y, Shindome, C, Takeda, M and Shiomi, K (2006) The roles of ERK and P38 MAPK signaling cascades on embryonic diapause initiation and termination of the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology 36, 47–53.CrossRefGoogle ScholarPubMed
Hao, K, Jie, W, Xiong-Bing, T, Whitman, DW and Zhang, ZH (2017) Transcriptomic and proteomic analysis of Locusta migratoria eggs at different embryonic stages: comparison for diapause and non-diapause regimes. Journal of Integrative Agriculture 16, 1777–1788.CrossRefGoogle Scholar
Joplin, KH and Denlinger, DL (1990) Developmental and tissue specific control of the heat shock induced 70 kDa related proteins in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology 36, 239–249.CrossRefGoogle Scholar
Kaupinis, A, Aitmanaitė, L, Strepetkaitė, D, Valius, M, Lazutka, JR and Arbačiauskas, K (2017) Proteomic and gene expression differences between post-diapause and subitaneous offspring phenotypes in the cyclic parthenogen Daphnia pulex. Hydrobiologia 798, 87–103.CrossRefGoogle Scholar
Kidokoro, K, Iwata, KI, Takeda, M and Fujiwara, Y (2006) Involvement of ERK/MAPK in regulation of diapause intensity in the false melon beetle, Atrachya menetriesi. Journal of Insect Physiology 52, 1189–1193.CrossRefGoogle ScholarPubMed
Kim, M and Denlinger, DL (2009) Decrease in expression of beta-tubulin and microtubule abundance in flight muscles during diapause in adults of Culex pipiens. Insect Molecular Biology 18, 295–302.CrossRefGoogle ScholarPubMed
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
Laemmli, UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Lawrence, M, Daujat, S and Schneider, R (2016) Lateral thinking: how histone modifications regulate gene expression. Trends in Genetics 32, 42–56.CrossRefGoogle ScholarPubMed
Ma, HY, Zhou, XR, Tan, Y and Pang, BP (2019) Proteomic analysis of adult Galeruca daurica (Coleoptera: Chrysomelidae) at different stages during summer diapause. Comparative Biochemistry and Physiology – Part D 29, 351–357.Google ScholarPubMed
MacRae, TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cellular and Molecular Life Sciences 67, 2405–2424.CrossRefGoogle ScholarPubMed
Masuda, H and Oliveira, PL (1985) Characterization of vitellin and vitellogenin from Rhodnius prolixus: identification of phosphorylated compounds in the molecule. Insect Biochemistry 15, 543–550.CrossRefGoogle Scholar
Peck, DC (2002) Distribución y reconocimiento del salivazo de los pastos (Homoptera: Cercopidae) en la Costa Caribe de Colombia. Pasturas Tropicales 24, 4–15.Google Scholar
Pereira, JF, Cunha, GRD and Moresco, ER (2019) Improved drought tolerance in wheat is required to unlock the production potential of the Brazilian Cerrado. Crop Breeding and Applied Biotechnology 19, 217–225.CrossRefGoogle Scholar
Ragland, GJ, Armbruster, PA and Meuti, ME (2019) Evolutionary and functional genetics of insect diapause: a call for greater integration. Current Opinion in Insect Science 36, 74–81.CrossRefGoogle Scholar
Ren, XY, Zhang, LS, Han, YH, An, T, Liu, Y, Li, YY and Chen, HY (2016) Proteomic research on diapause-related proteins in the female ladybird, Coccinella septempunctata L. Bulletin of Entomological Research 106, 168–174.CrossRefGoogle ScholarPubMed
Rinehart, JP and Denlinger, DL (2000) Heat-shock protein 90 is down-regulated during pupal diapause in the flesh fly, Sarcophaga crassipalpis, but remains responsive to thermal stress. Insect Molecular Biology 9, 641–645.CrossRefGoogle ScholarPubMed
Rinehart, JP, Yocum, GD and Denlinger, DL (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochemistry and Molecular Biology 30, 515–521.CrossRefGoogle ScholarPubMed
Rinehart, JP, Li, A, Yocum, GD, Robich, RM, Hayward, SA and Denlinger, DL (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences 104, 11130–11137.CrossRefGoogle ScholarPubMed
Rinehart, JP, Robich, RM and Denlinger, DL (2010) Isolation of diapause-regulated genes from the flesh fly, Sarcophaga crassipalpis by suppressive subtractive hybridization. Journal of Insect Physiology 56, 603–609.CrossRefGoogle ScholarPubMed
Shevchenko, A, Tomas, H, Havlis, J, Olsen, JV and Mann, M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature Protocols 1, 2856–2860.CrossRefGoogle ScholarPubMed
Silveira Neto, S, Nakano, O, Barbin, D and Vila Nova, NA (1976) Diapausa. In Manual de Ecologia de Insetos. Ed. Agron. Ceres Ltda. Piracicaba, pp. 70–75.Google Scholar
Storey, KB and Storey, JM (2012) Insect cold hardiness: metabolic, gene, and protein adaptation. Canadian Journal of Zoology 90, 456–475.CrossRefGoogle Scholar
Tachibana, SI, Numata, H and Goto, SG (2005) Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. Journal of Insect Physiology 51, 641–647.CrossRefGoogle ScholarPubMed
Tan, QQ, Liu, W, Zhu, F, Lei, CL, Hahn, DA and Wang, XP (2017) Describing the diapause-preparatory proteome of the beetle Colaphellus bowringi and identifying candidates affecting lipid accumulation using isobaric tags for mass spectrometry-based proteome quantification (iTRAQ). Frontiers in Physiology 8, 251.CrossRefGoogle Scholar
Tu, X, Wang, J, Hao, K, Whitman, DW, Fan, Y, Cao, G and 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.CrossRefGoogle Scholar
Valério, JR (2009) Cigarrinhas das pastagens. Campo Grande: Embrapa Gado de Corte, Documentos 179, 51 p.Google Scholar
Wolschin, F and Gadau, J (2009) Deciphering proteomic signatures of early diapause in Nasonia. PLoS ONE 4, e6394.CrossRefGoogle ScholarPubMed
Zhang, J and Storey, KB (2017) Insect cold hardiness: the role of mitogen-activated protein kinase and Akt signalling in freeze avoiding larvae of the goldenrod gall moth, Epiblema scudderiana. Insect Molecular Biology 26, 181–189.CrossRefGoogle ScholarPubMed
Zhang, Q, Lu, YX and Xu, WH (2012) Integrated proteomic and metabolomic analysis of larval brain associated with diapause induction and preparation in the cotton bollworm, Helicoverpa armigera. Journal of Proteome Research 11, 1042–1053.CrossRefGoogle ScholarPubMed
Zhang, C, Wei, D, Shi, G, Huang, X, Cheng, P, Liu, G, Guo, X, Liu, L, Wang, H, Miao, F and Gong, M (2019) Understanding the regulation of overwintering diapause molecular mechanisms in Culex pipiens pallens through comparative proteomics. Scientific Reports 9, 6485.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Saraiva et al. supplementary material

Saraiva et al. supplementary material 1

Download Saraiva et al. supplementary material(PDF)
PDF 262.8 KB
Supplementary material: PDF

Saraiva et al. supplementary material

Saraiva et al. supplementary material 2

Download Saraiva et al. supplementary material(PDF)
PDF 502.6 KB
Supplementary material: PDF

Saraiva et al. supplementary material

Saraiva et al. supplementary material 3

Download Saraiva et al. supplementary material(PDF)
PDF 1.1 MB
Supplementary material: PDF

Saraiva et al. supplementary material

Saraiva et al. supplementary material 4

Download Saraiva et al. supplementary material(PDF)
PDF 336.5 KB
Supplementary material: PDF

Saraiva et al. supplementary material

Saraiva et al. supplementary material 5

Download Saraiva et al. supplementary material(PDF)
PDF 331.3 KB