Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-09T09:20:18.173Z Has data issue: false hasContentIssue false
  • English
  • Français

ATP-binding cassette transporters ABCF2 and ABCG9 regulate rice black-streaked dwarf virus infection in its insect vector, Laodelphax striatellus (Fallén)

Published online by Cambridge University Press:  22 September 2021

Yuanxue Yang Open the ORCID record for Yuanxue Yang [Opens in a new window] ,
Aiyu Wang ,
Man Wang ,
Yun Zhang ,
Jianhua Zhang  and
Ming Zhao
Yuanxue Yang
Affiliation:
Institute of Industrial Crops, Shandong Academy of Agricultural Sciences, Jinan 250100, China
Aiyu Wang
Affiliation:
Institute of Industrial Crops, Shandong Academy of Agricultural Sciences, Jinan 250100, China
Man Wang
Affiliation:
Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
Yun Zhang*
Affiliation:
Institute of Industrial Crops, Shandong Academy of Agricultural Sciences, Jinan 250100, China
Jianhua Zhang*
Affiliation:
Institute of Industrial Crops, Shandong Academy of Agricultural Sciences, Jinan 250100, China Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
Ming Zhao*
Affiliation:
Institute of Industrial Crops, Shandong Academy of Agricultural Sciences, Jinan 250100, China
*
Authors for correspondence: Jianhua Zhang, Email: [email protected]; Ming Zhao, Email: [email protected]
Authors for correspondence: Jianhua Zhang, Email: [email protected]; Ming Zhao, Email: [email protected]
Authors for correspondence: Jianhua Zhang, Email: [email protected]; Ming Zhao, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The majority of plant viral disease is transmitted and spread by insect vectors in the field. The small brown planthopper, Laodelphax striatellus (Fallén), is the only efficient vector for rice black-streaked dwarf virus (RBSDV), a devastating plant virus that infects multiple grain crops, including rice, maize, and wheat. Adenosine triphosphate (ATP)-binding cassette (ABC) transporters participate in various biological processes. However, little is known about whether ABC transporters affect virus infection in insects. In this study, RBSDV accumulation was significantly reduced in L. striatellus after treatment with verapamil, an effective inhibitor of ABC transporters. Thirty-four ABC transporter genes were identified in L. striatellus and expression analysis showed that LsABCF2 and LsABCG9 were significantly upregulated and downregulated, respectively, after RBSDV infection. LsABCF2 and LsABCG9 were expressed during all developmental stages, and LsABCG9 was highly expressed in the midgut of L. striatellus. Knockdown of LsABCF2 promoted RBSDV accumulation, while knockdown of LsABCG9 suppressed RBSDV accumulation in L. striatellus. Our data showed that L. striatellus might upregulate the expression of LsABCF2 and downregulate LsABCG9 expression to suppress RBSDV infection. These results will contribute to understanding the effects of ABC transporters on virus transmission and provide theoretical basis for virus management in the field.

Keywords

ABC transportersABCF2ABCG9Laodelphax striatellusrice black-streaked dwarf virus
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 3 , June 2022 , pp. 327 - 334
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

Aurade, RM, Jayalakshmi, SK and Sreeramulu, K (2010) Modulatory effects of natural curcuminoids on P-glycoprotein ATPase of insecticide-resistant pest Helicoverpa armigera (Lepidopetera: Noctüidae). Journal of Membrane Biology 236, 271–278.CrossRefGoogle Scholar
Aurade, RM, Akbar, SM, Goud, H, Jayalakshmi, SK and Sreeramulu, K (2011) Inhibition of P-glycoprotein ATPase and its transport function of Helicoverpa armigera by morin, quercetin and phloroglucinol. Pesticide Biochemistry and Physiology 101, 212–219.CrossRefGoogle Scholar
Bao, L, Wu, J, Dodson, M, Montserrat, R, Ning, Y, Zhang, Z, Yao, M, Zhang, D, Xu, C and Yi, X (2017) ABCF2, An Nrf2 target gene, contributes to cisplatin resistance in ovarian cancer cells. Molecular Carcinogenesis 56, 1543–1553.CrossRefGoogle ScholarPubMed
Borycz, JA, Kubów, A, Lloyd, V and Meinertzhagen, IA (2008) Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. Journal of Experimental Biology 211, 3454–3466.CrossRefGoogle Scholar
Broehan, G, Kroeger, T, Lorenzen, M. and Merzendorfer, H (2013) Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics 14, 6.CrossRefGoogle ScholarPubMed
Choi, H, Ohyama, K, Kim, YY, Jin, JY, Lee, SB, Yamaoka, Y, Muranaka, T, Suh, MC, Fujioka, S and Lee, Y (2014) The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat. Plant Cell 26, 310–324.CrossRefGoogle ScholarPubMed
Davidson, AL, Assa, ED, Orelle, C and Chen, J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiology and Molecular Biology Reviews: MMBR 72, 317–364.CrossRefGoogle ScholarPubMed
Dean, M and Annilo, T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annual Review of Genomics and Human Genetics 6, 123–142.CrossRefGoogle ScholarPubMed
Derumauw, D and Leeuwen, TV (2014) The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochemistry and Molecular Biology 45, 89–110.CrossRefGoogle Scholar
Evans, JM, Day, JP, Cabrero, P, Dow, J and Davies, SA (2008) A new role for a classical gene: white transports cyclic GMP. Journal of Experimental Biology 211, 890–899.CrossRefGoogle ScholarPubMed
Gahan, LJ, Pauchet, Y, Vogel, H, Heckel, DG and Mauricio, R (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genetics 6, e1001248.CrossRefGoogle ScholarPubMed
Grbić, M, Leeuwen, TV, Clark, RM, Rombauts, S, Rouzé, P, Grbić, V, Osborne, EJ, Dermauw, W, Ngoc, PCT, Ortego, F, Hernandez-Crespo, P, Diaz, I, Martinez, M, Navajas, M, Sucena, E, Magalhaes, S, Nagy, L, Pace, RM, Djuranovic, S, Smagghe, G, Lga, M, Christianes, O, Veenstra, JA, Ewer, J, Villalobos, RM, Hutter, JL, Dudson, SD, Velez, M, Yi, SV, Zeng, J, Pires-daSiva, A, Roch, F, Cazaux, M, Navarro, M, Zhurov, V, Acevedo, G, Bjelica, A, Fawcett, JF, Bonnet, E, Martens, C, Baele, G, Wissler, L, Sachez-Rodiguez, A, Tirry, L, Blais, C, Demeestere, K, Henz, SR, Gregory, TR, Mathieu, J, Verdon, L, Farinelli, L, Schmutz, J, Lindquist, E, Fryerisen, R and Peer, YVD (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479, 487–492.CrossRefGoogle ScholarPubMed
Guo, ZJ, Kang, S, Chen, DF, Wu, QJ, Wang, SL, Xie, W, Zhu, X, Baxter, SW, Zhou, XG, Jurat-Fuentes, JL and Zhang, YJ (2015) MAPK Signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in diamondback moth. PLoS Genetics 11, e1005124.CrossRefGoogle ScholarPubMed
Guo, ZJ, Kang, S, Sun, D, Gong, LJ, Zhou, JL, Qin, JY, Guo, L, Zhu, LH, Bai, Y, Ye, F, Wu, QJ, Wang, SL, Crickmore, N, Zhou, XG and Zhang, YJ (2020) MAPK-dependent hormonal signaling plasticity contributes to overcoming Bacillus thuringiensis toxin action in an insect host. Nature Communications 11, 3003.CrossRefGoogle Scholar
He, C, Liang, J, Liu, S, Wang, S, Wu, Q, Xie, W and Zhang, Y (2018) Changes in the expression of four ABC transporter genes in response to imidacloprid in Bemisia tabaci Q (Hemiptera: Aleyrodidae). Pesticide Biochemistry and Physiology 153, 136–143.CrossRefGoogle Scholar
He, L, Chen, X, Yang, J, Zhang, TY, Li, J, Zhang, SB, Zhong, KL, Zhang, HM, Chen, JP and Yang, J (2020) Rice black-streaked dwarf virus-encoded P5-1 regulates the ubiquitination activity of SCF E3 ligases and inhibits jasmonate signaling to benefit its infection in rice. New Phytologist 225, 896–912.CrossRefGoogle ScholarPubMed
Hock, T, Cottrill, T, Keegan, J. and Garza, D (2000) The E23 early gene of Drosophila encodes an ecdysone-inducible ATP-binding cassette transporter capable of repressing ecdysone-mediated gene activation. Proceedings of the National Academy of Sciences 97, 9519–9524.CrossRefGoogle ScholarPubMed
Hogenhout, SA, Ammar, ED, Whitfield, AE and Redinbaugh, MG (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology 46, 327–359.CrossRefGoogle ScholarPubMed
Hollenstein, K, Dawson, RJ and Locher, KP (2007) Structure and mechanism of ABC transporter proteins. Current Opinion in Structural Biology 17, 412–418.CrossRefGoogle ScholarPubMed
Hopper-Borge, E, Xu, X, Shen, T, Shi, Z, Chen, ZS and Kruh, GD (2009) Human multidrug resistance protein 7 (ABCC10) is a resistance factor for nucleoside analogues and epothilone B. Cancer Research 69, 178–184.CrossRefGoogle ScholarPubMed
Itoh, TQ, Tanimura, T and Matsumoto, A (2011) Membrane-bound transporter controls the circadian transcription of clock genes in Drosophila. Genes to Cells 16, 1159–1167.CrossRefGoogle ScholarPubMed
Juan-Carlos, P, Perla-Lidia, PP, Stephanie-Talia, MM, Mónica-Griselda, A and Luz-María, T (2021) ABC transporter superfamily. An updated overview, relevance in cancer multidrug resistance and perspectives with personalized medicine. Molecular Biology Reports 48, 1883–1901.CrossRefGoogle ScholarPubMed
Kartner, N, Evernden-Porelle, D, Bradley, G and Ling, V (1985) Detection of P-glycoprotein in multidrug-resistant cell lines by monoclonal antibodies. Nature, 316, 820–823.CrossRefGoogle ScholarPubMed
Li, J, Xue, J, Zhang, HM, Yang, J, Lv, MF, Xie, L, Meng, Y, Li, PP and Chen, JP (2013) Interactions between the P6 and P5-1 proteins of southern rice black-streaked dwarf Fijivirus in yeast and plant cells. Archives of Virology 158, 1649–1659.CrossRefGoogle ScholarPubMed
Liu, S, Zhou, S, Tian, L, Guo, E and Sheng, L (2011) Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori. BMC Genomics 12, 491.CrossRefGoogle ScholarPubMed
Liu, XQ, Jiang, HB, Xiong, Y, Peng, P, Li, HF and Yuan, GR (2019) Genome-wide identification of ATP-binding cassette transporters and expression profiles in the Asian citrus psyllid, Diaphorina citri, exposed to imidacloprid. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 30, 305–311.Google ScholarPubMed
Lu, LN, Wang, Q, Huang, DQ, Xu, QF, Zhou, XP and Wu, JX (2019a) Rice black-streaked dwarf virus P10 suppresses protein kinase C in insect vector through changing the subcellular localization of LsRACK1. Philosophical Transactions of the Royal Society B-Biological Sciences 374, 20180315.CrossRefGoogle Scholar
Lu, G, Li, S, Zhou, CW, Qian, X, Xiang, Q, Yang, TQ, Wu, XJ, Zhou, XP, Zhou, YJ, Ding, X and Tao, XR (2019b) Tenuivirus utilizes its glycoprotein as a helper component to overcome insect midgut barriers for its circulative and propagative transmission. PLoS Pathogens 15, e1007655.CrossRefGoogle Scholar
Mackenzie, SM, Brooker, MR, Gill, TR, Cox, GB and Ewart, GD (1999) Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. Biochimica Biophysica Acta – Bioenergetics 1419, 173–185.CrossRefGoogle Scholar
Meng, XK, Yang, XM, Wu, ZL, Shen, QW, Miao, LJ, Zheng, Y, Qian, K and Wang, JJ (2020) Identification and transcriptional response of ATP-binding cassette transporters to chlorantraniliprole in the rice striped stem borer, Chilo suppressalis. Pest Management Science 76, 3626–3635.CrossRefGoogle ScholarPubMed
Morita, M and Imanaka, T (2012) Peroxisomal ABC transporters: structure, function and role in disease. Biochimica et Biophysica Acta 1822, 1387–1396.CrossRefGoogle Scholar
Rees, D, Johnson, E and Lewinson, O (2009) ABC transporters: the power to change. Nature Reviews Molecular Cell Biology 10, 218–227.CrossRefGoogle Scholar
Riordan, JR, Deuchars, K, Kartner, N, Alon, N, Trent, J and Ling, V (1985) Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 316, 817–819.CrossRefGoogle ScholarPubMed
Rosner, J, Tietmeyer, J and Merzendorfer, H (2021) Functional analysis of ABCG and ABCH transporters from the red flour beetle, Tribolium castaneum. Pest Management Science 77, 2955–2963.CrossRefGoogle ScholarPubMed
Shan, J, Sun, X, Li, R, Zhu, B, Liang, P and Gao, X (2021) Identification of ABCG transporter genes associated with chlorantraniliprole resistance in Plutella xylostella (L.). Pest Management Science 77, 3491–3499.CrossRefGoogle ScholarPubMed
Sun, LY, Xie, L, Andika, IB, Tan, ZL and Chen, JP (2013) Non-structural protein P6 encoded by rice black-streaked dwarf virus is recruited to viral inclusion bodies by binding to the viroplasm matrix protein P9-1. Journal of General Virology 94, 1908–1916.CrossRefGoogle Scholar
Wenzel, JJ (2007) ABC A-subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport. Frontiers in Bioscience 12, 8–12.CrossRefGoogle ScholarPubMed
Wu, N, Zhang, L, Ren, YD and Wang, XF (2020) Rice black-streaked dwarf virus: from multiparty interactions among plant-virus-vector to intermittent epidemics. Molecular Plant Pathology 21, 1007–1019.CrossRefGoogle ScholarPubMed
Xiao, LF, Zhang, W, Jing, TX, Zhang, MY, Miao, ZQ, Wei, DD, Yuan, GR and Wang, JJ (2018) Genome-wide identification, phylogenetic analysis, and expression profiles of ATP-binding cassette transporter genes in the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Comparative Biochemistry and Physiology D-Genomics and Proteomics 25, 1–8.CrossRefGoogle Scholar
Yang, H, Zhou, C, Yang, XB, Long, GY and Jin, DC (2019) Effects of insecticide stress on expression of NlABCG transporter gene in the brown planthopper, Nilaparvata lugens. Insects 10, 334.CrossRefGoogle ScholarPubMed
Zhang, HM, Chen, JP and Adams, MJ (2001) Molecular characterisation of segments 1 to 6 of rice black-streaked dwarf virus from China provides the complete genome. Archives of Virology 146, 2331–2339.CrossRefGoogle ScholarPubMed
Zhang, HH, Tan, XX, He, YQ, Xie, KL, Li, LL, Wang, R, Hong, GJ, Li, J, Taliansky, M, MacFarlane, S, Yan, F, Chen, JP and Sun, ZT (2019) Rice black-streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus. Molecular Plant Pathology 20, 641–655.CrossRefGoogle ScholarPubMed
Zhu, JJ, Jiang, F, Wang, XH, Yang, PC, Bao, YY, Zhao, W, Wang, W, Lu, H, Wang, QS, Cui, N, Li, J, Chen, XF, Luo, L, Yu, JT, Kang, L and Cui, F (2017) Genome sequence of the small brown planthopper Laodelphax striatellus. Gigascience 6, 1–12.CrossRefGoogle ScholarPubMed
Zutz, A, Gompf, S, Schägger, H and Tampé, R (2009) Mitochondrial ABC proteins in health and disease. Biochimica et Biophysica Acta 1787, 681–690.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Yang et al. supplementary material

Figure S1

Download Yang et al. supplementary material(Image)
Image 110.2 KB
Supplementary material: File

Yang et al. supplementary material

Table S1

Download Yang et al. supplementary material(File)
File 12.2 KB