   )-

ļœŜ, Ğ©ñÄń¥ÌŘŧù Ņ¾ƢķŞÌŘŧLmNo
230-0045 ŝÆÚŕħĳÜǑƖ¦ėáŊ 1-7-22
Naoyoshi Kumakura, Yukio Kurihara
Link between plant virus and RNA silencing
Key words: plant RNA virus, resistance, RNA silencing, symptom
RIKEN Center for Sustainable Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama,Kanagawa, 230-0045 Japan
DOI: 10.24480/bsj-review.8b3.00113
*1 "5=<jJ,(ýüó),£ĠĿ#ÃŌ&"5£Ŀ), ünü©ªò'}Ǝ65ōĨĤ8tï'=<jJ(¿ĭ8ǁ,RNA ßĴnG<kmImCĨĤǓĠĿ#( RNA ßĴ8 RNA G<kmImC$²/, ĘŤ#) RNA ßĴ8°/" RNA G<kmImC$²ş5ǔ8jJýüó'$)š#5pď#, ĠĿ) RNA G<kmIC"ƹƔ&è¡8¨/"5 RNA G<kmImC)·ó(ƲÊƶ$Ŕ¯&ƶ8Á(ŐŃû=<36"-ãƻ$&5$$3Ô5$, (ƲÊŃơ#51998 à'ŹƊ#, xĘƽ RNAÊc@WKb(pŨRNA ßĴ(/"»±6 ǓFire et al. 1998ǔĠĿ#(Ńơ(ŐƖ) 1990 à'Ʊ5_PfW:#·óƲÊ$Ŕ¯&ƲÊ8æƣƨĄ#Ô5$, (ƲÊ(ŐŃû65$mImC(/"(»±#5$žđ3'&4, 6

Ńơ$"( RNA G<k36"5 (Napoli et al. 1990)(*æƣƨĄĠĿ#ÔƲÊ( RNA G<kmImC'25û

(2', *.36"Ń·#),RNA G<kmImC$), űſ'Ë·5ƾ 21-24 ½ºŢâ(ÕÊ RNAŔƑŒ&ƶ8ÿ! RNA 'Ŵ®, RISC (RNA-induced silencing complex) $²*65?\>BNoƓ®
8iBjoT5$# RNA (Ƙn-)Žƚû8ƌ
$&

c@WKb#5$đ3"5 ǓChapman and Carrington 2007, Iwakawa and Tomari 2015ǔŖğņĿ'"

RNA G<kmImC(ŐņnŅ¾òũ'5è¡)ǉÞ'ƹƔ#4, RNA G<kmIm
 &$#&%  &%"!%  % '" (      C(!

(uƔ&ƲÊ8ĩĆņĿ), £ĠĿ´7Ƅī'ƃ5ƹŬ&ƎŃ¹8Śŀ'ĠĿ'
üó'"), ŐņưŢnJTkJòũĒ(ƲÊŐŃ(ín=<jJý"ƹƔ#5$đ3'&"5ĘŤ#)6-#đ3

ĠĿ( RNA G<kmImC8, ĠĿ=<jJýüĨĤ$"(Ǌ'&"3ģƞ5 RNA G<kmImC)Ãx!(JRQ^'365ÕÊ RNA (ņ®÷$, ÕÊ RNA '25ĦŒ RNA ,(Ň#5ÕÊ RNA )ƾ 21-24 ½ºŢâ( RNA #4,ņ®÷ưŢ(3 microRNA (miRNA) $ small interfering RNA (siRNA) 'Ǐ65miRNAǐ)EYb'FoU6, mRNA $¯ĥ' RNA `ichoM II '2

ėŨ'AeQ^Ĥƭ$ 3ʹ`i A ėŨ8ÿ!Ǔ¶ 1, ­ǔmiRNAƑó"ƨ6, 5ʹǐ)ƂƧ(ƶ(ÿ!Ŕ

3JRbjo^Ĥƭ8æ÷, xĘƽ RNA ĎƷŰ#5 Dicer-like 1 (DCL1) '2
ƜƠ6, Īř' miRNA $&5ƶ465 (Kurihara and Watanabe

2004, Kurihara et al. 2006)÷Ľ miRNA )ğ3ğÁ,$Š£, ŔƑŒ&ĦŒ RNA"(Ĥƭ8û5$ž36"5miRNA (ÿ!ŀî$"), EYb'FoU6"5$,miRNA (ĦŒ$&5 mRNA (ţǏİ-"5$#5 pď, 21 ½ºƾ( siRNA ) miRNA $Ō&4,EYbq(ƶ'ǃ3ÁĚƲÊ&%Âĥ
&ƶ80$'®÷6521-22 nt ƾ( siRNA (ǐ$&5 RNA )űſƣ# SGS3 $2*65Nm[Bƣ'Ŵ®, xĘƽ RNA ®÷ƷŰ#5 RDR6 '2"xĘƽ¥65(Dalmay et al. 2000, Mourrain et al. 2000, Peragine et al. 2004, Yoshikawa et al. 2005)SGS3 $RDR6 )űſƣ# SGS3/RDR6-body (siRNA-body) $2*65ǎŭŁĤƭ8æ÷5$
(Ĥƭ# siRNA (ǐxĘƽ RNA ¥65$ž

3,365 (Jouannet et al. 2012,Kumakura et al. 2009)(xĘƽ RNA )xĘƽ RNA ĎƷŰ#5 Dicer-like Nm[Bƣ'2"Ũ

3 21-22 nt ƾ!ǌ'Ď6, ÷Ľ siRNA $&5(2©č), =<jJňĚ( RNA, űſƣ#Ƙ6&siRNA) (ǐ&%ÂØ'75(& siRNA ( mRNA, ta-siRNA (trans-actingŀî#5 (Allen et al. 2005, Hamilton and Baulcombe

1999, Gazzani et al. 2004)
 ņ®÷ųƦ$)Ō&4 siRNA 1 miRNA (ŇĨĤ)Ƭ"5dSjĠĿ#5Il<XVKV) RISC (Ĳótï#5 Argonaute (AGO) $²*65 endonuclease Ĳó8ÿ!
Nm[Bƣ8 11 ţFoU5AGO ) siRNAnmiRNA $Ŵ®5`DQT8

"4, «4ƪ9 siRNAnmiRNA $ŔƑŒ&ƶ8ÿ!ĦŒ RNA 8Ď5), (Žƚ8û5miRNAŴ®5()u' AGO1 #5siRNA ) AGO1-11 (665AGO1-11 )ŐŃn×·([NomŌ&"4, %( AGO $Ŵ®530ġ) miRNAnsiRNA (Ň8ŗ5#ǉÞ'ƹƔ#5ĠĿ#)ÕÊ RNA ( 5ʹėŨ(½ºAGO '«4ƪ-658İ/5ƹƔ&µÊ#5$

đ3'&"5$%(*, &$#&%  &%"!%  % '" (      AGO2 )u' 5ʹėŨ':SWm8ÿ!ÕÊ RNA $, AGO5 )u' 5ʹėŨ'ITIm8ÿ!
ÕÊ RNA ) AGO5 $Ŵ®5(2'ÕÊ RNA )66Ɨ³ó8ÿ! AGO $Ŵ®, ĦŒ RNA 'Ň5 (Mi et al. 2008, Takeda et al. 2008)

RNA "5)-^hJƽ RNA =<jJ8

4&$RNA G<kmImC)ĠĿ=<jJ(¿ĭ8û5ýüóĨĤ$"pď#ĠĿ=<jJ)@=mNoS;\>mJ$" RNA G<kmImC8ǂÐ5ûµÊ8Ƃ3"5=<jJňĚ( siRNA )=<jJ RNA 8Ƙ5#)&Ñu(ŔƑŒ& mRNA 0Ƙ"-Ŏî

Ń65$ž

3653'=<jJ(ûµÊ)miRNA ųƦ0ǂÐ"-miRNA $(ĦŒmRNA (ZhmJ8Ù"-Ŏî8ãƤ)-'!# ŗ36"5ĠĿ=<jJ(Ů¡)EYbRNA

3&5 RNA =<jJ#4, (EYb RNA )ÁƏNm[Bƣ'ƕ76"5=<jJ(ÁƏNm[Bƣ8ŐŃ5ŲĄĠĿ), =<jJ(öĝn¿ĭ'Ò"ýüó8Ś$

ŗ36" (Abel et al. 1986)

-, ĠĿ=<jJ(öĝ8vǁ5/', v/ĠĿ'Ŏ©ó(ääĮ=<jJ8öĝ", ë3"5åĮ=<jJ(öĝ8ǁúı0á76"(Kurihara and Watanabe, 2003)1990 à}(ë§', qƙ(2kmImC(Ǐó&=<jJýüó$ RNA G<Āć6É/ (Ratcliff et al. 1997)", 1999 à(=<jJňĚ( &$#&%  &%"!%  % '" (      siRNA (ŐƖ'2",RNA G<kmImC=<jJ'Ò5ýüóĨĤ#5$Ŗ'ƛđ6(#5 (Hamilton and Baulcombe 1999)
ĠĿ=<jJ$ RNA G<kmImC'25ýüó(ÊĨĤ'!", #)NZFd
H<B=<jJ (TMV) '}Ǝ65^hJƽ RNA =<jJ8TMV EYb)^hJƽ(pĘƽ RNA #4, 6'Ƙƞ5 (¶ 1, Û)

ÁƏNm[Bƣ'¤-65$#=<jJŭÊ8æ÷"5(=<jJ)űſ'5$ÁƏNm[Bƣb RNA

Á6, EY3ĠĿ(ÿ!ŽƚƐż8Ň"ƓƒƷŰ(Žƚ8ƿÉ5ƓƒƷŰ), ^hJƽ

#5EYb RNA3a<VJƽ RNAǓxĘƽ¥ǔ8®÷, 3'a<VJƽ RNA 8Ƽ

¹'EYb RNA 8Ɠƒ5(2'pĘƽ^hJƽ RNA xĘƽ¥$a<VJƽ RNA8Ƽ¹'^hJƽ RNA (®÷(pƮ(G<Bj8Ż4ƫ$#=<jJ)ľŐŒ'¿ĭ5pď#ĠĿ), =<jJ(¿ĭ8û

5/', =<jJƓƒĒ(xĘƽ RNA (Dicer '25Ď8Ƭ", RNA G<kmImC8+Ƥ=<jJňĚ( siRNA (ņ÷5 (Hamilton and Baulcombe 1999)siRNA ņ÷) RDR1/6 (Ň'2", 3'Ư65(Wang et al. 2010)ņ÷6 siRNA ), 3'=<jJ RNA 8ĦŒ$"Ƙ5$#,¿ĭ8û 5$ž36"5, =<jJ0ĠĿ'136"*4#)&=<jJ)ƂƧ(EYbq' RNA G<kmImCĨĤ8û5Nm[Bƣ8FoU5ƲÊ8ÿ!(#5Ǔ¶ 1, tÅǔĔ'¯Ï6=<jJ(ûµÊ)`R;=<jJ'FoU6 HC-Pro (helpercomponent protease) #5 (Anandalakshmi et al. 1998, Kasschau and Carrington, 1998)0$0$ HC-Pro ), ƾĕ'75=<jJ(EYbƓƒ1, ŶūęËŒ&=<jJ(ƾƥǈŠƌ'ðƔ&µÊ$"ŗ36"63(Ńơ) HC-Pro

RNA G<kmImC8ǂÐ5$#ãƤ65-, áŗ36"5ûµÊ$") P19FoU5 19 kDa Nm[Bƣ#, =<jJ'$

ZJ=<jJ5P19 )Tm"Ŏî8ãƤ('ðƔ&µÊ$"¯Ï6, ë'űſ( siRNA $Ŵ®,( siRNA ( RISC ,(«4ƪ.8ǂÐ5$#, RNA G<kmImC8û5$đ3'&

 (Silhavy et al. 2002,

Qiu et al. 2002, Qu and Morris 2002)įƩŒƆƘĜ6"5 P19 '25 RNA G<kmImCû(p8¶ 2 'ŚŴēĤƭƘĜ'2", P19 )pŲ( siRNA duplexǓ¶ 1ǔ'Ò"ƶ')Ë'O<ao$"Ŵ®5$2003)(2&óƣ3, P19 ) siRNA duplex $¯Ĥƭ8ÿ! miRNA duplex '0Ŵ®5HC-Pro 1 P19 (.&3, ĥ&=<jJ3(Â»±6"5 (Vargason et al.

ÕÊ RNA $Ŵ®5$ûµÊ8ÿ!$đ3'&4, 6Ś6 (Lakatos et al. 2006, Merai et al. 2006,Voinnet et al. 1999) 'ā TMV (¼®,ƓƒƷŰ,=<jJ(Ɠƒ8þ#)&, &$#&%  &%"!%  % '" (      ÕÊ RNA 'Ŵ®5$# RNA G<kmImCûµÊ$"0 (Csorba et al. 2007,
Kubota et al. 2003, Kurihara et al. 2007)p!(Nm[Bƣ), =<jJ(ƆŪRISCĢ/"Ö&ƲÊõ»(.#ĔÃǃ(Ĩƀ8Őą, ņË5/(¢ł

06&(2'ĠĿ=<jJ)ûµÊ8ŐŃ5$#ÕÊ RNA 83ǆǈ, ƂƧ(EYb RNA 8 RNA G<kmImCĨĤ<kmImC8û5$652

Ō&5x!(Ĩƀ80!$'&, ĠĿ=<jJ'$3Î

"5RNA G")pƅŒ&öĝøŋ#5$ž

3"  P19
'RNA 

ôÞŒ' GFP 8ŐŃ5 Nicotiana benthamiana (ƈ'Á33' GFP ƲÊ8Ô5$ GFP ƋƵ50((, RNA G<kmImC

Ɩ36

ƝŐ65/äƋ$&5 (Û)pď#, GFP ƲÊ$$0' p19 ƲÊ8
Ô5$ RNA G<kmImC)û6, å GFP ƋƖ365Ǔ­ǔ:Cl<m\;jTkoIgmı8Ň"ƲÊÔ8ƌŖ) UV ĻÓr#Ĉç,+0%

4& =<jJ)ĠĿ'öĝ, Ƨ'á

"Ŏî8ãƤĠĿűſ'öĝ=<jJ), űſ#Ɠƒ6, ©æƣƮŵ8Ƭư"űſĝűſ

3ǈ6Ųź,$á3űſ,$Š£, Ýū8{", ö"=<jJöĝČů'}Ǝ65Ųź(Ƈ(À¥&%įƩŒŦ1&0(űſī&%(Ĺ0(-#ÂØ'7563(ŎîãƤ6"5)ĖƘđ(ƵjJ( RNA G<kmImCûµÊ
đ3'&Â

&ãƤŎî)dH<Bĥ
3, ŐņưŢ,(Ã&çǋ1%(2&c@WKb'2"

3, Ö&$0pƵ(Ŏî),=<, miRNA ųƦ8ǂÐ5$#ãƤ65$"5 `R;=<jJ#5@]dH<B=<jJ (TuMV)
ƾǂÐ1ĹŐņŌÞ$Ŏî

Il<XVKV'öĝ5$ņ

Ń65TuMV )ûµÊ#5 HC-Pro 8FoU"4, HC-Pro 8ŐŃIl<XVKV), TuMV öĝĠĿ$Ǐ÷ƾ(ǂÐ8¬HC-Pro ŐŃĠĿ$ TuMV öĝĠĿ#)Ƭ", ƓĊ( miRNA (ĦŒ$65 mRNA (ƉťqĐ"!-4, HC-ProsiRNA ųƦ8û5#)&, miRNA ųƦ0 &$#&%  &%"!%  % '" (      ǂÐ5$

3', miRNA (ĦŒ mRNA (Â)Őņ8í5µÊǓƨ

7µÊ&%ǔ8FoU5$3, miRNA ųƦǂÐ6, ĦŒ mRNA (ƺŒ&¸ƍ

5$'24, TuMV (Ŏî(pƵ$"ŐņŌÞet al., 2003)miRNA ųƦ(ǂÐ'2ãƤ65$žÙ636 (Kasschau"ãƤ65ŐņŌÞǓŎîǔ), ƓĊ(ûµÊ8'ŐŃ5Il<XVKV#.36$3, =<jJŎ'ƬŎîŐņc06& (Chapman et al. 2004)

@WKb&(', =<jJňĚ siRNA ), ĺ'0 siRNA (ƶ'ŔƑŒ&ÑuǓĠĿǔ ¶Ǖ'Ś2

( mRNA 8Ƙ(ĦŒ$5$ž365ĠĿ=<jJ'|ǅ"Ë·5GRh<T RNA $²*65Nm[Bƣ8FoU&Ŏ©ó RNA

5Af=idG<B=<jJǓCMVǔ'|ǅ"Ë·5GRh<T RNAǓY-satǔ), NZF', Y-sat ňĚ( siRNAƤ(Ŏî(©µ"ǒ¥(ŎîãBll\;j(ņ÷'ðǍ(·óƲ

Ê#5 CHL1 ( mRNA 8Ƙnû"5/#5$Ś6 (Shimura et al. 2011,Smith et al. 2011)
 ¯ĥ(Ńơ,=<jJ'Ǐ=<l<U$(Ñu'"»±6"5=<l<U), pĘƽŅŁ RNA (EYb8ÿ, Nm[Bƣ8FoU&ĠĿűſ#ƂêŒ'¿ĭ, =<jJ¯ĥ'Ŏî8ãƤ(=<l<U(Ŏî%(26"5'2)ƾà(Ɵ#" siRNA'ã=<l<U0=<jJ¯ĥ'ĠĿ( RNA G<kmImC

ņ÷6û65 (Hammann and Steger 2012, Wang et al. 2004)ddĸ·dH<B=<l<UǓPLMVdǔdd'öĝ5$, ƈ'ő¥(ŏŁ

=<l<UňĚ(x!( siRNAƈŸ(ņ®÷'ǀ75 cHSP90 ( mRNA 8Ƙnû"5/#5$=<l<UňĚ( siRNA

Ń65(Ŏî0,Ś6 (Navarro et al. 2012)~q(»±~Á'0, =<jJ-)Ñu( mRNA 8ĦŒ$"5$"5 (Hammann and Steger 2012, Miozzi et al. 2012)

&ăĶ65»±&63, -ġƛ6)Ö&/, zë(»±8é





ƾĕ'75ĠĿ=<jJ$Ñu(ýüó'ǀ5Řŧ(t#, RNA G<kmImC
ÁĚóğƸ'Ò5ûĨĤ#5$<kmImCĨĤ'2ûµÊ8Ƃ3"¿ĭđ3$&ĠĿ=<jJ)Ñu( RNA Gû65pď#, =<jJ)(ýü8û5/("53', 63( RNA G<kmImCûµÊ)ÑuƲÊ(ŐŃíĨĤ'ßĴ, Ŏî8ãƤ=<jJŎ)Ē', ÑuÊÍ8Ĭ$8È

5$05=<jJ'$Ë·5¼"),Ñu'ưâ&Ŏî

Ń6, Ƃ3Ɓ &$#&%  &%"!%  % '" (      6"-$)ĘĚÇ-&RNA G<kmImC$=<jJ

ýü(ǀ),-ZhmJ8$4&

3Ư¥"(0!ûµÊ'25

06&

23
 ĠĿ( RNA Řŧ, ŀ' RNA G<kmImC'ǀ5Řŧ'ìw5Ĩ8s"ěyÃÌÃÌǄŷ®ċ¥ŘŧŞ(ĵƳǇpƴĉĂ'(¼84"íśŉq-$/(.Abel, P. P., Nelson, R. S., De, B., Hoffmann, N., Rogers, S. G., Fraley, R. T., and Beachy, R. N. 1986.
Delay of disease development in transgenic plants that express the tobacco mosaic virus
coat protein gene. Science 232: 738-743.
Allen, E., Xie, Z., Gustafson, A. M., and Carrington, J. C. 2005. microRNA-directed phasing duringtrans-acting siRNA biogenesis in plants. Cell 121: 207-221.
Anandalakshmi, R., Pruss, G.J., Ge, X., Marathe, R., Mallory, A. C., Smith, T. H., and Vance, V. B.
1998. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. USA 95: 13079–13084.
Chapman, E. J., and Carrington, J. C. 2007. Specialization and evolution of endogenous small RNA
pathways. Nat. Rev. Genet. 8: 884-894.
Chapman, E. J., Prokhnevsky, A. I., Gopinath, K., Dolja, V. V., and Carrington, J. C. 2004. Viral RNA
silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev.
18: 1179-1186.
Csorba, T., Bovi, A., Dalmay, T., and Burgyan, J. 2007. The p122 subunit of tobacco mosaic virus
replicase is a potent silencing suppressor and compromises both small interfering RNAand microRNA-mediated pathways. J. Virol. 81: 11768-11780.
Dalmay, T., Hamilton, A., Rubb, S., Angell, S., and Baulcombe, D. C. 2000. An RNA-dependent RNA
polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediatedby a transgene but not by a virus. Cell 101: 543-553.
Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A. Driver, S. E., and Mello, C. C. 1998. Potent andspecific interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:
806-811.
Gazzani, S., Lawrenson, T., Woodward, C., Headon, D., and Sablowski, R. 2004. A link between
mRNA turnover and RNA interference in Arabidopsis. Science 306: 1046-1048.
Hamilton, A. J., and Baulcombe, D. C. 1999. A species of small antisense RNA in posttranscriptional
gene silencing in plants. Science 286: 950-952.
Hammann, C., and Steger, G. 2012. Viroid-specific small RNA in plant disease. RNA Biol. 9:809-819.

 &$#&%  &%"!%  % '" (      

Iwakawa, H. O., and Tomari, Y. 2015. The functions of microRNAs: mRNA decay and translational
repression. Trends Cell Biol. 25: 651-665.
Jouannet, V., Moreno, A. B., Elmayan, T., Vaucheret, H., Crespi, M. D., and Maizel, A. 2012.
Cytoplasmic Arabidopsis AGO7 accumulates in membrane associated siRNA bodies and isrequired for ta siRNA biogenesis. EMBO J. 31: 1704–1713.
Kasschau, K. D., and Carrington, J. C. 1998. A Counterdefensive strategy of plant viruses: suppressionof posttranscriptional gene silencing. Cell 95: 461–470.
Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A., and Carrington, J. C.
2003. P1/HC-Pro, a Viral suppressor of RNA silencing, interferes with Arabidopsisdevelopment and miRNA function. Dev. Cell 4: 205–217.
Kubota, K., Tsuda, S., Tamai, A., and Meshi, T. 2003. Tomato mosaic virus replication protein
suppresses virus-targeted posttranscriptional gene silencing. J. Virol. 77: 11016-11026.
Kumakura, N., Takeda, A., Fujioka, Y., Motose, H., Takano, R., and Watanabe, Y. 2009. SGS3 andRDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett. 583: 1261–1266.
Kurihara, Y., Inaba, N., Kutsuna, N., Takeda, A., Tagami, Y., and Watanabe, Y. 2007. The binding oftobamovirus replication protein with small RNA duplexes. J. Gen. Virol. 88: 2347-2352.
Kurihara, Y., Takashi, Y., and Watanabe, Y. 2006. The interaction between DCL1 and HYL1 isimportant for efficient and precise processing of pri-miRNA in plant microRNA biogenesis.
RNA 12: 206–212.
Kurihara, Y., and Watanabe, Y. 2003. Cross-protection in Arabidopsis against crucifer tobamovirus Cg
by an attenuated strain of the virus. Mol. Plant Pathol. 4: 259-269.
Kurihara, Y., and Watanabe, Y. 2004. Arabidopsis micro-RNA biogenesis through Dicer-like 1 proteinfunctions. Proc. Natl. Acad. Sci. USA 101: 12753–12758.
Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., Liu, Y. P., Dolja, V. V., Calvino,L. F., Lopez-Moya, J. J., and Burgyan, J. 2006. Small RNA binding is a common strategy
to suppress RNA silencing by several viral suppressors. EMBO J. 25: 2768-2780.
Merai, Z., Kerenyi, Z., Kertesz, S., Magna, M., Lakatos, L., and Silhavy, D. 2006. Double-stranded
RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J.
Virol. 80: 5747-5756.
Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Wu, L., Li, S., Zhou, H., Long, C., et al. 2008.
Sorting of small RNAs into Arabidopsis argonaute complexes Is directed by the 5 terminal
nucleotide. Cell 133: 116–127.
Miozzi, L., Gambino, G., Burgyan, J., Pantaleo, V. 2013. Genome-wide identification of viral and hosttranscripts targeted by viral siRNAs in Vitis vinifera. Mol. Plant Pathol. 14: 30-43.
Mourrain, P., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J. B., Jouette, A. M., Nikic, S.,Picault, N., Remoue, K., et al. 2000. Arabidopsis SGS2 and SGS3 genes are required for
 &$#&%  &%"!%  % '" (      

posttranscriptional gene silencing and natural virus resistance. Cell 101: 533-542.
Napoli, C., Lemieux, C., and Jorgensen, R. 1990. Introduction of a chimeric Chalcone Synthase Gene
into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289.
Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H. L., and Poethig, R. S. 2004. SGS3 andSGS2/SDE1/RDR6 are required for juvenile development and the production oftrans-acting siRNAs in Arabidopsis. Genes Dev. 18: 2368–2379.
Qiu, W., Park, J. W., and Scholthof, H. B. 2002. Tombusvirus P19-Mediated Suppression ofVirus-Induced Gene Silencing Is Controlled by Genetic and Dosage Features That
Influence Pathogenicity. Mol. Plant. Microbe Interact. 15: 269–280.
Qu, F., and Morris, T. J. 2002. Efficient infection of Nicotiana benthamiana by tomato bushy stunt
virus is facilitated by the coat protein and maintained by p19 through suppression of genesilencing. Mol. Plant. Microbe Interact. 15: 193–202.
Ratcliff, F., Harrison, B. D., and Baulcombe, D. C. 1997. A similarity between viral defense and genesilencing in plants. Science 276: 1558-1560.
Shimura, H., Pantaleo, V., Ishihara, T., Myojo, N., Inaba, J., Sueda, K., Burgyan, J., and Masuta, C.
2011. A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene
involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog. 7:e1002021.
Silhavy, D., Molnár, A., Lucioli, A., Szittya, G., Hornyik, C., Tavazza, M., and Burgyán, J. 2002. Aviral protein suppresses RNA silencing and binds silencing  generated, 21- to
25-nucleotide double-stranded RNAs. EMBO J. 21: 3070–3080.
Smith, N. A., Eamens, A. L., and Wang, M. B. 2011. Viral small interfering RNAs target host genes tomediate disease symptoms in plants. PLoS Pathog. 7: e1002022.
Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., and Watanabe, Y. 2008. The mechanism selecting
the guide strand from small RNA duplexes is different among argonaute proteins. Plant
Cell Physiol. 49: 493–500.
Vargason, J. M., Szittya, G., Burgyán, J., and Hall, T. M. T. 2003. Size Selective Recognition of siRNAby an RNA Silencing Suppressor. Cell 115: 799–811.
Voinnet, O., Pinto, Y. M., and Baulcombe, D. C. 1999. Suppression of gene silencing: A general
strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96:14147–14152.
Wang, M.-B., Bian, X.-Y., Wu, L.-M., Liu, L.-X., Smith, N. A., Isenegger, D., Wu, R.-M., Masuta, C.,
Vance, V. B., Watson, J. M., Rezaian, A., Dennis, E. S., and Waterhouse, P. M. 2004. On therole of RNA silencing in the pathogenicity and evolution of viroids and viral satellites.
Proc. Natl. Acad. Sci. USA 101: 3275-3280.
Wang, X.B., Wu, Q., Ito, T., Cillo, F., Li, W.X., Chen, X., Yu, J.L.&Ding, S.W. 2010.

 &$#&%  &%"!%  % '" (      

RNAi-mediated viral immunity requires amplification of virus-derived siRNAs inArabidopsis thaliana. Proc Natl Acad Sci USA 107: 484–489.
Yoshikawa, M., Peragine, A., Park, M. Y., and Poethig, R. S. 2005. A pathway for the biogenesis oftrans-acting siRNAs in Arabidopsis. Genes Dev. 19: 2164–2175.

 &$#&%  &%"!%  % '" (   