Role of aminopeptidase N-like in the acquisition of begomoviruses by Bemisia tabaci, the whitefly vector

Abstract

Sri Lankan cassava mosaic virus (SLCMV) is a prominent causative agent of cassava mosaic disease in Asia and relies on the whitefly Bemisia tabaci cryptic complex for its transmission. However, the molecular mechanisms involved in SLCMV transmission by B. tabaci have yet to be understood. In this study, we identified an aminopeptidase N-like protein (BtAPN) in B. tabaci Asia II 1, an efficient vector of SLCMV, which is involved in the SLCMV transmission process. Through the use of glutathione S-transferase pull-down assay and LC-MS/MS analysis, we demonstrated the interaction between BtAPN and the coat protein (CP) of SLCMV. This interaction was further confirmed in vitro, and we observed an induction of BtAPN gene expression following SLCMV infection. By interfering with the function of BtAPN, the quantities of SLCMV were significantly reduced in various parts of B. tabaci Asia II 1, including the whole body, midgut, hemolymph, and primary salivary gland. Furthermore, we discovered that BtAPN is conserved in B. tabaci Middle East-Asia Minor 1 (MEAM1) and interacts with the CP of tomato yellow leaf curl virus (TYLCV), a begomovirus known to cause severe damage to tomato production. Blocking BtAPN with antibody led to a significant reduction in the quantities of TYLCV in whitefly whole body and organs/tissues. These results demonstrate that BtAPN plays a generic role in interacting with the CP of begomoviruses and positively regulates their acquisition by the whitefly.

Keywords

BtAPN / coat protein / SLCMV / TYLCV / virus acquisition / whitefly

References

[1] Chi,Y., Pan,L.L., Bouvaine,S., Fan, Y.Y., Liu,Y.Q., Liu,S.S. et al. (2020) Differential transmission of Sri Lankan cassava mosaic virus by three cryptic species of the whitefly Bemisia tabaci complex. Virology, 540, 141–149.

[2] Chittarath,K., Jimenez, J., Vongphachanh,P., Leiva,A.M., Sengsay, S., Lopez-Alvarez,D. et al. (2021) First report of Sri Lankan cassava mosaic virus and cassava mosaic disease in Laos. Plant Disease, 105, 1861.

[3] Czosnek,H., Hariton-Shalev, A., Sobol,I., Gorovits,R. and Ghanim, M. (2017) The incredible journey of begomoviruses in their whitefly vector. Viruses, 9, 273.

[4] Delmas,B., Gelfi,J., L'Haridon,R., Vogel,L.K., Sjöström, H., Norén,O. et al. (1992) Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature, 357, 417–420.

[5] Fiallo-Olivé,E., Lett, J.M., Martin,D.P., Roumagnac,P., Varsani, A., Zerbini,F.M. et al. (2021) ICTV virus taxonomy profile: Geminiviridae 2021. Journal of General Virology, 102, 001696.

[6] Fiallo-Olivé,E., Pan, L.L., Liu,S.S. and Navas-Castillo,J. (2020) Transmission of begomoviruses and other whitefly-borne viruses: dependence on the vector species. Phytopathology, 110, 10–17.

[7] Ghanim,M., Morin,S. and Czosnek,H. (2001) Rate of tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology, 91, 188–196.

[8] He,Y.Z., Wang,Y.M., Yin,T.Y., Cuellar, W.J., Liu,S.S. and Wang,X.W. (2021) Gut-expressed vitellogenin facilitates the movement of a plant virus across the midgut wall in its insect vector. mSystems, 6, e00521–e00581.

[9] Hemniam,N., Roekwan, S., Vannatim,N., Malichan,S., Saokham, K., Chaowongdee,S. et al. (2022) Natural infection of Cnidoscolus and Jatropha by Sri Lankan cassava mosaic virus in Thailand. Journal of General Plant Pathology, 88, 386–391.

[10] Hogenhout,S.A., Ammar,E., Whitfield,A.E. and Redinbaugh,M.G. (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology, 46, 327–359.

[11] Jose,A., Makeshkumar, T. and Edison,S. (2008) Host range of Sri Lankan cassava mosaic virus. Journal of Root Crops, 34, 21–25.

[12] Kanakala,S. and Ghanim, M. (2019) Global genetic diversity and geographical distribution of Bemisia tabaci and its bacterial endosymbionts. PLoS ONE, 14, e0213946.

[13] Lefeuvre,P., Martin, D.P., Harkins,G., Lemey,P., Gray,A.J., Meredith,S. et al. (2010) The spread of tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathogens, 6, e1001164.

[14] Legg,J.P., Lava Kumar, P., Makeshkumar,T., Tripathi,L., Ferguson, M., Kanju,E. et al. (2015) Cassava virus diseases: biology, epidemiology, and management. Advances in Virus Research, 91, 85–142.

[15] Li,B.X., Ge,J.W. and Li,Y.J. (2007) Porcine aminopeptidase N is a functional receptor for the PEDV coronavirus. Virology, 365, 166–172.

[16] Li,M., Hu,J., Xu,F.C. and Liu, S.S. (2010) Transmission of tomato yellow leaf curl virus by two invasive biotypes and a Chinese indigenous biotype of the whitefly Bemisia tabaci. International Journal of Pest Management, 56, 275–280.

[17] Liu,S.S., Colvin, J. and De Barro,P.J. (2012) Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? Journal of Integrative Agriculture, 11, 176–186.

[18] Mugerwa,H., Colvin, J., Alicai,T., Omongo,C.A., Kabaalu, R., Visendi,P. et al. (2021) Genetic diversity of whitefly (Bemisia spp.) on crop and uncultivated plants in Uganda: implications for the control of this devastating pest species complex in Africa. Journal of Pest Science, 94, 1307–1330.

[19] Pan,L.L., Chen,Q.F., Zhao,J.J., Guo, T., Wang,X.W., Hariton-Shalev,A. et al. (2017) Clathrin-mediated endocytosis is involved in tomato yellow leaf curl virus transport across the midgut barrier of its whitefly vector. Virology, 502, 152–159.

[20] Qin,L., Wang,J., Bing,X.L. and Liu, S.S. (2013) Identification of nine cryptic species of Bemisia tabaci (Hemiptera: Aleyrodidae) from China by using the mtCOI PCR-RFLP technique. Acta Entomologica Sinica, 56, 186–194.

[21] Rey,C. and Vanderschuren, H. (2017) Cassava mosaic and brown streak diseases: current perspectives and beyond. Annual Review of Virology, 4, 429–452.

[22] Roumagnac,P., Lett,J.M., Fiallo-Olive,E., Navas-Castillo,J., Zerbini, F.M., Martin,D.P. et al. (2022) Establishment of five new genera in the family Geminiviridae: Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus. Archives of Virology, 167, 695–710.

[23] Saokham,K., Hemniam, N., Roekwan,S., Hunsawattanakul,S., Thawinampan, J. and Siriwan,W. (2021) Survey and molecular detection of Sri Lankan cassava mosaic virus in Thailand. PLoS ONE, 16, e0252846.

[24] Thresh,J.M. and Cooter, R.J. (2005) Strategies for controlling cassava mosaic virus disease in Africa. Plant Pathology, 54, 587–614.

[25] Tresnan,D.B., Levis,R. and Holmes,K.V. (1996) Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. Journal of Virology, 70, 8669–8674.

[26] Uke,A., Hoat,T.X., Quan,M.V., Liem, N.V., Ugaki,M. and Natsuaki,K.T. (2018) First report of Sri Lankan cassava mosaic virus infecting cassava in Vietnam. Plant Disease, 102, 2669–2670.

[27] Wang,B., Liu,Y., Ji,C.M., Yang, Y.L., Liang,Q.Z., Zhao,P. et al. (2018) Porcine deltacoronavirus engages the transmissible gastroenteritis virus functional receptor porcine aminopeptidase N for infectious cellular entry. Journal of Virology, 92, e00318.

[28] Wang,D., Yao,X.M., Huang,G.X., Shi, T., Wang,G.F. and Ye,J. (2019) First report of Sri Lankan cassava mosaic virus infected cassava in China. Plant Disease, 103, 1437–1438.

[29] Wang,H.L., Cui,X.Y., Wang,X.W., Liu, S.S. and Zhou,X.P. (2015) First report of Sri Lankan cassava mosaic virus infecting cassava in Cambodia. Plant Disease, 100, 1029.

[30] Wang,X.W. and Blanc, S. (2021) Insect transmission of plant single-stranded DNA viruses. Annual Review of Entomology, 66, 389–405.

[31] Whitfield,A.E., Falk,B.W. and Rotenberg,D. (2015) Insect vector-mediated transmission of plant viruses. Virology, 479−480, 278–289.

[32] Xia,W.Q., Liang,Y., Chi,Y., Pan, L.L., Zhao,J., Liu,S.S. et al. (2018) Intracellular trafficking of begomoviruses in the midgut cells of their insect vector. PLoS Pathogens, 14, e1006866.

[33] Xie,Y., Zhou,X.P., Zhang,Z.K. and Qi, Y.J. (2002) Tobacco curly shoot virus isolated in Yunnan is a distinct species of Begomovirus. Chinese Science Bulletin, 47, 197–200.

[34] Yang,Y.L., Liu,J., Wang,T.Y., Chen, M., Wang,G., Yang,Y.B. et al. (2021) Aminopeptidase N is an entry co-factor triggering porcine deltacoronavirus entry via an endocytotic pathway. Journal of Virology, 95, e0094421.

[35] Yeager,C.L., Ashmun, R.A., Williams,R.K., Cardellichio,C.B., Shapiro, L.H., Look,A.T. et al. (1992) Human aminopeptidase N is a receptor for human coronavirus 229E. Nature, 357, 420–422.

[36] Zang,L.S., Liu,Y.Q. and Liu,S.S. (2005) A new clip-cage for whitefly experimental studies. Chinese Bulletin of Entomology, 42, 329–333.

[37] Zhao,J., Lei,T., Zhang,X.J., Yin, T.Y., Wang,X.W. and Liu,S.S. (2020) A vector whitefly endocytic receptor facilitates the entry of begomoviruses into its midgut cells via binding to virion capsid proteins. PLoS Pathogens, 16, e1009053.

RIGHTS & PERMISSIONS

2024 2024 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.