title: Rice stripe tenuivirus nonstructural protein 3 hijacks the 26S proteasome of the small brown planthopper via direct interaction with regulatory particle non-ATPase subunit 3.
abstract: The ubiquitin/26S proteasome system plays a vital role in regulating host defenses against pathogens. Previous studies have highlighted different roles for the ubiquitin/26S proteasome in defense during virus infection in both mammals and plants, but their role in the vectors that transmit those viruses is still unclear. In this study, we determined that the 26S proteasome is present in the small brown planthopper (SBPH) (Laodelphax striatellus) and has components similar to those in plants and mammals. There was an increase in the accumulation of Rice stripe virus (RSV) in the transmitting vector SBPH after disrupting the 26S proteasome, indicating that the SBPH 26S proteasome plays a role in defense against RSV infection by regulating RSV accumulation. Yeast two-hybrid analysis determined that a subunit of the 26S proteasome, named RPN3, could interact with RSV NS3. Transient overexpression of RPN3 had no effect on the RNA silencing suppressor activity of RSV NS3. However, NS3 could inhibit the ability of SBPH rpn3 to complement an rpn3 mutation in yeast. Our findings also indicate that the direct interaction between RPN3 and NS3 was responsible for inhibiting the complementation ability of RPN3. In vivo, we found an accumulation of ubiquitinated protein in SBPH tissues where the RSV titer was high, and silencing of rpn3 resulted in malfunction of the SBPH proteasome-mediated proteolysis. Consequently, viruliferous SBPH in which RPN3 was repressed transmitted the virus more effectively as a result of higher accumulation of RSV. Our results suggest that the RSV NS3 protein is able to hijack the 26S proteasome in SBPH via a direct interaction with the RPN3 subunit to attenuate the host defense response.
  
  
  OBJECTIVE
  We show, for the first time, that the 26S proteasome components are present in the small brown planthopper and play a role in defense against its vectored plant virus (RSV). In turn, RSV encodes a protein that subverts the SBPH 26S proteasome via direct interaction with the 26S proteasome subunit RPN3. Our results imply that the molecular arms race observed in plant hosts can be extended to the insect vector that transmits those viruses.
authors: State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China.
authors: Yi
authors: Y
authors: Xu
authors: State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China.
authors: Jianxiang
authors: J
authors: Wu
authors: State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China.
authors: Shuai
authors: S
authors: Fu
authors: State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China.
authors: Chenyang
authors: C
authors: Li
authors: State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China.
authors: Zeng-Rong
authors: ZR
authors: Zhu
authors: State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People's Republic of China zzhou@zju.edu.cn.
authors: Xueping
authors: X
authors: Zhou
mesh_terms: D000818:Animals; D001483:Base Sequence; D015153:Blotting, Western; D005982:Glutathione Transferase; D006430:Hemiptera / Q000235:genetics / Q000378:metabolism* / Q000821:virology*; D054884:Host-Pathogen Interactions; D008969:Molecular Sequence Data; D010957:Plasmids / Q000235:genetics; D046988:Proteasome Endopeptidase Complex / Q000235:genetics / Q000378:metabolism*; D034622:RNA Interference; D017422:Sequence Analysis, DNA; D029364:Tenuivirus / Q000235:genetics / Q000378:metabolism*; D017361:Viral Nonstructural Proteins / Q000378:metabolism*; D001616:beta-Galactosidase
chemical_list: D017361:Viral Nonstructural Proteins; D005982:Glutathione Transferase; D001616:beta-Galactosidase; D046988:Proteasome Endopeptidase Complex; C061553:ATP dependent 26S protease
references: Annu Rev Biochem. 2009;78:477-513
references: 19489727
references: Virus Genes. 2005 Oct;31(2):211-21
references: 16025247
references: Biochemistry. 2001 Jan 16;40(2):314-9
references: 11148024
references: PLoS One. 2012;7(9):e46238
references: 23029445
references: Annu Rev Phytopathol. 1998;36:139-63
references: 15012496
references: J Gen Virol. 2002 Dec;83(Pt 12):3187-97
references: 12466497
references: J Mol Biol. 2011 Jul 15;410(3):383-99
references: 21619884
references: J Virol. 2008 Dec;82(24):12304-11
references: 18818319
references: Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18649-54
references: 21949367
references: Mol Cell Biol. 1999 Oct;19(10):6872-90
references: 10490625
references: J Gen Virol. 2005 Sep;86(Pt 9):2595-603
references: 16099919
references: J Virol. 2007 Dec;81(23):12881-8
references: 17898064
references: J Biol Chem. 2008 Nov 14;283(46):31813-22
references: 18796432
references: Annu Rev Phytopathol. 1996;34:249-74
references: 15012543
references: Biochem J. 2004 Feb 15;378(Pt 1):177-84
references: 14583091
references: Mol Plant. 2014 Apr;7(4):691-708
references: 24214893
references: Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13079-84
references: 9789044
references: J Virol. 2014 Mar;88(6):3223-34
references: 24390331
references: J Gen Virol. 1994 Mar;75 ( Pt 3):467-75
references: 8126445
references: Mol Reprod Dev. 2000 Oct;57(2):176-84
references: 10984418
references: J Virol. 2012 Dec;86(24):13486-500
references: 23035235
references: Plant Physiol. 2006 Dec;142(4):1642-55
references: 17041027
references: Science. 2002 Oct 18;298(5593):611-5
references: 12183636
references: PLoS One. 2012;7(12):e52546
references: 23300704
references: Curr Opin Biotechnol. 2001 Apr;12(2):150-4
references: 11287229
references: J Virol. 2000 Apr;74(7):3330-7
references: 10708450
references: Mol Plant Pathol. 2011 Oct;12(8):808-14
references: 21726383
references: Science. 1986 Oct 10;234(4773):179-86
references: 3018930
references: J Virol. 2014 May;88(10):5437-43
references: 24574411
references: J Biol Chem. 1993 Aug 15;268(23):17413-7
references: 8349624
references: Annu Rev Biophys Biomol Struct. 1998;27:133-64
references: 9646865
references: Virology. 2012 Apr 10;425(2):113-21
references: 22305130
references: J Biol Chem. 1987 Jun 15;262(17):8303-13
references: 3298229
references: PLoS Biol. 2006 Aug;4(8):e267
references: 16869714
references: Plant Cell. 2011 Jan;23(1):273-88
references: 21245466
references: Cell Death Differ. 2005 Sep;12(9):1167-77
references: 16094393
references: Nature. 2008 May 22;453(7194):548-52
references: 18497827
references: Mol Cell Biol. 2005 Jun;25(11):4662-75
references: 15899868
references: Acta Virol. 2012;56(1):75-9
references: 22404613
references: Mol Cells. 2012 Jan;33(1):43-51
references: 22134721
references: Plant Physiol. 2011 Nov;157(3):1394-406
references: 21885668
references: Oncogene. 1999 Jan 14;18(2):449-58
references: 9927201
references: Virology. 2009 Apr 25;387(1):29-40
references: 19251298
references: Front Plant Sci. 2012 Dec 07;3:269
references: 23233857
references: Nat Rev Mol Cell Biol. 2009 Feb;10(2):104-15
references: 19165213
references: PLoS One. 2014;9(2):e88636
references: 24523924
references: PLoS One. 2013;8(8):e70357
references: 23936414
references: Virus Res. 2014 Apr;183:112-6
references: 24560843
references: Plant Cell. 2010 Sep;22(9):3142-52
references: 20823192
references: Nature. 2008 May 22;453(7194):481-8
references: 18497817
references: J Gen Virol. 2009 Apr;90(Pt 4):1025-34
references: 19264655
references: J Mol Biol. 2010 Dec 10;404(4):665-79
references: 20951141
references: PLoS One. 2012;7(4):e36238
references: 22558400
references: J Virol Methods. 2014 Jan;195:134-40
references: 24121134
references: BMC Genomics. 2010;11:400
references: 20573269
references: Proc Natl Acad Sci U S A. 2014 Apr 15;111(15):5544-9
references: 24706844
references: Virol Sin. 2012 Apr;27(2):100-8
references: 22492001
references: BMC Genomics. 2010;11:303
references: 20462456
references: Virol J. 2013;10:310
references: 24139455
references: Plant J. 2010 May;62(3):463-72
references: 20128884
references: Trends Biochem Sci. 1998 Jul;23(7):244-5
references: 9697412