Analysis of the roles of MAD proteins in the wing dimorphism of Nilaparvata lugens.
IIS‐FoxO pathway
Nilaparvata lugens
Nlmad1
Nlmad2
wing dimorphism
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
03 Jul 2024
03 Jul 2024
Historique:
revised:
15
05
2024
received:
06
03
2024
accepted:
21
05
2024
medline:
4
7
2024
pubmed:
4
7
2024
entrez:
3
7
2024
Statut:
aheadofprint
Résumé
Wing dimorphism in Nilaparvata lugens is controlled by the insulin-like growth factor 1 (IGF-1) signaling - Forkhead transcription factors (IIS-FoxO) pathway. However, the role of this signal in the wing development program remains largely unclear. Here, we identified 2 R-SMAD proteins, NlMAD1 and NlMAD2, in the brown planthopper (BPH) transcriptome, derived from the intrinsic transforming growth factor-β pathway of insect wing development. Both proteins share high sequence similarity and conserved domains. Phylogenetic analysis placed them in the R-SMAD group and revealed related insect orthologs. The expression of Nlmad1 was elevated in the late instar stages of the macropterous BPH strain. Nlmad1 knockdown in nymphs results in malformed wings and reduced wing size in adults, which affects the forewing membrane. By contrast, Nlmad2 expression was relatively consistent across BPH strains and different developmental stages. Nlmad2 knockdown had a milder effect on wing morphology and mainly affected forewing veins and cuticle thickness in the brachypterous strain. NlMAD1 functions downstream of the IIS-FoxO pathway by mediating the FoxO-regulated vestigial transcription and wing morph switching. Inhibiting Nlmad1 partially reversed the long-winged phenotype caused by NlFoxO knockdown. These findings indicate that NlMAD1 and NlMAD2 play distinct roles in regulating wing development and morph differentiation in BPH. Generally, NlMAD1 is a key mediator of the IIS-FoxO pathway in wing morph switching.
Identifiants
pubmed: 38961475
doi: 10.1111/1744-7917.13409
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
ID : 32172396
Informations de copyright
© 2024 Institute of Zoology, Chinese Academy of Sciences.
Références
Aashaq, S., Batool, A., Mir, S.A., Beigh, M.A., Andrabi, K.I. and Shah, Z.A. (2021) TGF‐β signaling: a recap of SMAD‐independent and SMAD‐dependent pathways. Journal of Cellular Physiology, 237, 59–85.
Alarcón, C., Zaromytidou, A.I., Xi, Q.R., Gao, S., Yu, J.Z., Fujisawa, S. et al. (2009) Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF‐β pathways. Cell, 139, 757–769.
Datto, M.B., Li, Y., Panus, J.F., Howe, D.J., Xiong, Y. and Wang, X.F. (1995) Transforming growth factor beta induces the cyclin‐dependent kinase inhibitor p21 through a p53‐independent mechanism. Proceedings of the National Academy of Sciences USA, 92, 5545–5549.
Denno, R.F. and Roderick, G.K. (1992) Density‐related dispersal in planthoppers: effects of interspecific crowding. Ecology, 73, 1323–1334
Edgar, B.A., Britton, J., de la Cruz, A.F., Johnston, L.A., Lehman, D., Martin‐Castellanos, C. et al. (2001) Pattern‐ and growth‐linked cell cycles in Drosophila development. Novartis Foundation Symposium, 237, 3–12.
Gomis, R.R., Alarcón, C., He, W., Wang, Q., Seoane, J., Lash, A. et al. (2006) A FoxO‐Smad synexpression group in human keratinocytes. Proceedings of the National Academy of Sciences USA, 103, 12747–12752.
Graff, J.M., Bansal, A. and Melton, D.A. (1996) Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell, 85, 479–487.
Hannon, G.J. and Beach, D. (1994) p15INK4B is a potential effector of TGF‐β‐induced cell cycle arrest. Nature, 15, 257–261.
Harrison, R.G. (1980) Dispersal polymorphisms in insects. Annual Review of Ecology and Systematics, 11, 95–118.
Hevia, C.F., López‐Varea, A., Esteban, N. and de Celis, J.F. (2017) A search for genes mediating the growth‐promoting function of TGFβ in the Drosophila melanogaster wing disc. Genetics, 206, 231–249.
Hill, C.S. (2009) Nucleocytoplasmic shuttling of Smad proteins. Cell Research, 19, 36–46.
Hoodless, P.A., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M.B., Attisano, L. et al. (1996) MADR1, a MAD‐related protein that functions in BMP2 signaling pathways. Cell, 85, 489–500.
Kim, J., Johnson, K., Chen, H.J., Carroll, S. and Laughon, A. (1997) Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature, 388, 304–308.
Kingsley, D.M. (1994) The TGF‐β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Development, 8, 133–146.
Lee, K.L., Lim, S.K., Orlov, Y.L., Yit, L.Y., Yang, H., Ang, L.T. et al. (2011) Graded Nodal/Activin signaling titrates conversion of quantitative phospho‐Smad2 levels into qualitative embryonic stem cell fate decisions. PLoS Genetics, 7, e1002130.
Liu, F., Li, K., Li, J., Hu, D., Zhao, J., He, Y. et al. (2015) Apterous A modulates wing size, bristle formation and patterning in Nilaparvata lugens. Scientific Reports, 5, 10526.
Liu, F., Li, X., Zhao, M., Guo, M., Han, K., Dong, X. et al. (2020) Ultrabithorax is a key regulator for the dimorphism of wings, a main cause for the outbreak of planthoppers in rice. National Science Review, 7, 1181–1189.
Li, X., Zhao, M.H., Tian, M.M., Zhao, J., Cai, W.L. and Hua, H.X. (2021) An InR/mir‐9a/NlUbx regulatory cascade regulates wing diphenism in brown planthoppers. Insect Science, 28, 1300–1313.
Lin, X., Chen, Y., Meng, A. and Feng, X. (2007) Termination of TGF‐β superfamily signaling through SMAD dephosphorylation‐a functional genomic view. Journal of Genetics and Genomics, 34, 1–9.
Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real‐time quantitative PCR and the 2−ΔΔCt Method. Methods (San Diego, Calif.), 25, 402–408.
Marchler‐Bauer, A., Derbyshire, M.K., Gonzales, N.R., Lu, S., Chitsaz, F., Geer, L.Y. et al. (2015) CDD: NCBI's conserved domain database. Nucleic Acids Research, 43, D222–D226.
Massagué, J. (1998) TGF‐β signal transduction. Annual Review of Biochemistry, 67, 753–791.
Matsumura, M. (1996) Genetic analysis of a threshold trait: density‐dependent wing dimorphism in Sogatella furcifera (Horvath) (Hemiptera: Delphacidae), the whitebacked planthopper. Heredity, 76, 229–237
Morooka, S., Ishibashi, N. and Tojo, S. (2008) Relationship between wing‐form response to nymphal density and black colouration of adult body in the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Applied Entomology and Zoology, 23, 449–458.
Newfeld, S.J., Chartoff, E.H., Graff, J.M., Melton, D.A. and Gelbart, W.M. (1997) Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF‐β responsive cells. Development (Cambridge, England), 122, 2099–2108.
Pierreux, C.E., Nicolás, F.J. and Hill, C.S. (2000) Transforming growth factor β‐independent shuttling of Smad4 between the cytoplasm and nucleus. Molecular and Cellular Biology, 20, 9041–9054.
Raftery, L.A., Twombly, V., Wharton, K., Gelbart, W.M. (1995) Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics, 139, 241–254.
Reynisdóttir, I. and Massagué, J. (1997) The subcellular locations of p15 (Ink4b) and p27(Kip1) coordinate their inhibitory interactions with cdk4 and cdk2. Genes & Development, 11, 492–503.
Reynisdóttir, I., Polyak, K., Iavarone, A. and Massagué, J. (1995) Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF‐β. Genes & Development, 9, 1831–1845.
Roff, D.A. (1991) Life‐history consequences of bioenergetic and biomechanical constraints on migration. American Zoologist, 31, 205–215.
Ross, S. and Hill, C.S. (2008) How the Smads regulate transcription. The International Journal of Biochemistry & Cell Biology, 40, 383–408.
Sekelsky, J.J., Newfeld, S.J., Raftery, L.A., Chartoff, E.H., Gelbart, W.M. (1995) Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics, 139, 1347–1358.
Seoane, J., Le, H.V., Shen, L., Anderson, S.A. and Massagué, J. (2004) Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell, 117, 211–223.
Shi, Y.G. and Massagué, J. (2003) Mechanisms of TGF‐β signaling from cell membrane to the nucleus. Cell, 113, 685–700.
Thompson, J.D., Gibson, T.J. and Higgins, D.G. (2002) Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, 2, 2–3.
Watanabe, M., Masuyama, N., Fukuda, M. and Nishida, E. (2000) Regulation of intracellular dynamics of Smad4 by its leucine‐rich nuclear export signal. European Molecular Biology Organization Reports, 1, 176–182.
Wu, G., Chen, Y.G., Ozdamar, B., Gyuricza, C.A., Chong, P.A., Wrana, J.L. et al. (2000) Structural basis of Smad2 recognition by the Smad anchor for receptor activation. Science, 287, 92–97.
Wu, J.W., Hu, M., Chai, J., Seoane, J., Huse, M., Li, C. et al. (2001) Crystal structure of a phosphorylated Smad2: Recognition of phosphoserine by the MH2 domain and insights on Smad function in TGF‐β signaling. Molecular Cell, 8, 1277–1289.
Xiao, Z., Brownawell, A.M., Macara, I.G. and Lodish, H.F. (2003a) A novel nuclear export signal in Smad1 is essential for its signaling activity. Journal of Biological Chemistry, 278, 34245–34252.
Xiao, Z., Latek, R. and Lodish, H.F. (2003b) An extended bipartite nuclear localization signal in Smad4 is required for its nuclear import and transcriptional activity. Oncogene, 22, 1057–1069.
Xiao, Z., Liu, X., Henis, Y.I. and Lodish, H.F. (2000) A distinct nuclear localization signal in the N terminus of Smad 3 determines its ligand‐induced nuclear translocation. Proceedings of the National Academy of Sciences USA, 97, 7853–7858.
Xiao, Z., Watson, N., Rodriguez, C. and Lodish, H.F. (2001) Nucleocytoplasmic shuttling of Smad1 conferred by its nuclear localization and nuclear export signals. Journal of Biological Chemistry, 276, 39404–39410.
Xu, H.J., Xue, J., Lu, B., Zhang, X.C., Zhuo, J.C., He, S.F. et al. (2015) Two insulin receptors determine alternative wing morphs in planthoppers. Nature, 519, 464–467.
Zera, A.J. and Denno, R.F. (1997) Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology, 42, 207–230.
Zhang, J.L., Fu, S.J., Chen, S.J., Chen, H.H., Liu, Y.L., Liu, X.Y. et al. (2021) Vestigial mediates the effect of insulin signaling pathway on wing‐morph switching in planthoppers. PLoS Genetics, 9, e1009312.
Zhang, C., Mao, M.S. and Liu, X.D. (2022) Relative contribution of genetic and environmental factors to determination of wing morphs of the brown planthopper Nilaparvata lugens. Insect Science, 30, 208–220.