Current Opinion in Microbiology 2003, 6:406–409 www.current-opinion.

c om
Plnt !"# $iru% e$olution
Mrilyn & !oo%%inc'
!"# $iru%e% re t(e mo%t common $iru%e% o) plnt%, n* t(e
e$olution o) t(e%e $iru%e% (% been %tu*ie* bot( e+perimentlly
n* p(ylogeneticlly. ,(e b%ic moleculr mec(ni%m% )or plnt
$iru% e$olution re %imilr to t(o%e o) ot(er $iru%e%, wit( %ome
notble e+ception%. !ecent *$nce% inclu*e new in%ig(t% into
t(e origin% o) plnt $iru%e%, nly%e% o) -u%i%pecie% n*
muttion )re-uencie%, popultion %tu*ie% on )iel* i%olte% n*
prcticl %tu*ie% on t(e importnce o) $iru% e$olution to
griculture.
#**re%%e%
Plnt .iology /i$i%ion, ,(e 0muel !obert% "oble 1oun*tion,
#r*more, O2 33402, 40#
e-mil: mroo%%i n c'5noble.org
Current Opinion in Microbiology 2003, 6:406–409
,(i% re$iew come% )rom t(eme* i%%ue on
6o%t–microbe interction%: $iru%e%
7*ite* by 7%tebn /omingo
8369-9234:; – %ee )ront mtter
2003 7l%e$ier 0cience <t*. #ll rig(t% re%er$e*.
/O= 80.8086:08369-9234>03?000@3-0
#bbre$ition%
CMA Cucumber mo%ic $iru%
MP mo$ement protein
=ntro*uction
#lt(oug( t(e e$olution o) !"# $iru%e% (% been mo%t
t(oroug(ly %tu*ie* in niml %y%tem%, in recent yer%
plnt $iru%e% ($e gine* more prominent plce in
t(e )iel*. Plnt $iru%e% ($e been u%e* % mo*el %y%tem%
)or $iru% e$olution B8C becu%e o) t(e ob$iou% *$ntge o)
u%ing plnt% % (o%t%: no niml %y%tem cn pro$i*e
unlimite* number% o) geneticlly i*enticl (o%t% )or
in)ectionD plnt protopl%t% pro$i*e primry cell culture
%y%tem t(t $oi*% %ome o) t(e pit)ll% o) niml ti%%ue
cultureD n* t(ere re no et(icl concern% bout *oing
w(ole plnt e+periment%. =n **ition, t(e prcticl impor-
tnce to griculture in un*er%tn*ing $iru% e$olution (%
been recogniEe*, e%pecilly in lig(t o) concern% bout t(e
%)ety o) geneticlly mo*i)ie* orgni%m%, n* becu%e
plnt $iru% re%i%tnce (% not lwy% pro$en %tble un*er
)iel* con*ition%.
Plnt% l%o pre%ent )ew notble *i))erence% )rom niml%
in reltion to t(e e$olution o) $iru%e%. Plnt cell% ($e
wll% w(o%e connection% re re%tricte*, n* %ucce%%)ul
$iru% mu%t e$ol$e mec(ni%m% to mo$e t(roug(out t(e
plnt. 6ence, t(ere re no FlyticG in)ection% in plnt%, n*
406
common term% li'e Fbur%t %iEeG re not mening)ul. Plnt%
re not mobile, %o $iru%e% mu%t l%o e$ol$e %trtegie% )or
(o%t-to-(o%t %pre*. Plnt% *o not ($e n immune %y%-
tem t(t *pt% to pt(ogen% li'e niml% *o, but ($e
in%te* *e$elope* bot( %peci)ic n* non%peci)ic *e)en%e
re%pon%e% to $iru%e%.
,(ere ($e been )ew e+perimentl e$olution %tu*ie%
reporte* )or plnt !"# $iru%e%, but t(e mHority o)
current wor' coul* be con%i*ere* lrgely
*e%cripti$e. ,(i% inclu*e% p(ylogenetic nly%e% o)
e+tnt $iru%e% in n e))ort to un*er%tn* t(eir
e$olutionry (i%tory, n* com- prti$e %tu*ie% o)
popultion% o) plnt $iru%e% )rom )iel* %mple%.
Popultion %tu*ie% ($e generlly been limite* to
compri%on% o) in*i$i*ul i%olte% n* t(ere (% been
little nly%i% o) popultion $rition wit(in %ingle
i%olte% >or -u%i%pecie%?, out%i*e o) e+perimentl
popultion%.
=t i% not t(e intention o) t(i% re$iew to be compre(en%i$e,
but rt(er to co$er t(e mo%t %igni)icnt contribution% to
t(e )iel* o) plnt !"# $iru% e$olution t(t ($e occurre*
o$er t(e p%t two yer%. !e*er% will be *irecte* to ot(er
recent re$iew% )or more compre(en%i$e re*ing on
relte* %ubHect%. =n **ition, t(i% re$iew will co$er t(e-
oreticl mo*el% o) $iru% e$olution in lig(t o) t(e en*o-
%ymbiotic reltion%(ip o) $iru%e% wit( ec( ot(er n* t(eir
(o%t plnt%.
Origin% n* c-ui%ition o) new gene%
,(e origin o) plnt $iru%e% remin% ob%cure. ,(e $%t
mHority o) plnt $iru%e% re %ingle-%trn*e* !"# $iru%e%
wit( plu%-%en%e polrity. ,(ere re l%o %mll /"#
$iru%e% in plnt%, n* prretro$iru%e%, but no lrge
/"# $iru%e% ($e % yet been i*enti)ie* )rom plnt%.
!ecently, %e$erl prretro$iru%e% o) plnt% ($e been
)oun* integrte* into plnt genome%. 0ome o) t(e%e cn
be cti$te* n* *e$elop epi%oml in)ection% un*er
(ybri* con*ition% B2

C, implying t(e e+i%tence o) repre%-
%or in t(e genome o) t(e plnt t(t crrie% t(e $irl
%e-uence%, t(t i% %ome(ow rele%e* *uring (ybri*iEtion
o) t(e plnt%.
0ome plnt $iru%e% )ll into bro* t+onomic group% t(t
inclu*e in%ect n*:or niml $iru%e%, %ugge%ting com-
mon origin. Plnt $iru%e% re mo%t o)ten trn%mitte* by
in%ect% n* t(i% (% le* to t(e %pecultion t(t t(e
progenitor% o) bot( plnt n* niml $iru%e% mig(t ($e
been in%ect $iru%e%. 6owe$er, ot(er plnt $iru%e% ($e
more in common wit( )ungl $iru%e%, mo%t notbly t(e
plnt cryptic $iru%e% B3C. Cryptic $iru%e% re *ouble-
%trn*e* !"# $iru%e% t(t ($e been )oun* in $irtully
e$ery plnt w(ere t(ey ($e been loo'e* )or, *e%pite
Plnt !"# $iru% e$olution !oo%%inc' 2
t(eir low titer n* lc' o) (oriEontl trn%mi%%ion w(ic(
m'e% t(em *i))icult to *etect. =n plnt%, t(e%e $iru%e% re
trn%mitte* $erticlly n* re unble to mo$e )rom cell to
cell, %pre*ing t(roug(out t(e plnt only by cell *i$i%ion.
,(e lc' o) in)ormtion bout bot( cryptic plnt $iru%e%
n* )ungl $iru%e% m'e% t(oroug( nly%i% *i))icult, but
t(e en*o%ymbiotic reltion%(ip between plnt% n* en*o-
p(ytic )ungi pro$i*e% $e(icle )or cro%%-'ing*om trn%-
mi%%ion. 6ence, plnt cryptic $iru%e% mig(t be )ungl
$iru%e% t(t ($e e%cpe* t(eir norml (o%t *uring n
en*op(ytic %%ocition, but re unble to replicte e))i-
ciently or mo$e, lc'ing t(e pproprite mo$ement pro-
tein% >MP%?. =*entity between t(e !"#-*epen*ent !"#
polymer%e o) )ungl $iru%e% n* plnt cryptic $iru%e%
%upport% t(i% (ypot(e%i% >M& !oo%%inc', unpubli%(e*
*t?. Plnt% e+pre%% protein% t(t )unction li'e $irl
MP% >e.g. 2notte*8 B4C?, %%ociting wit( pl%m*e%mtl
%tructure% n* )cilitting t(e mo$ement o) !"#
between plnt cell%. Plnt $iru%e% mig(t ($e *pte*
by c-uiring t(eir MP% )rom t(eir (o%t%. ,(e %imilrity
between $irl MP% i% $ery low, e$en wit(in )mily w(ere
t(e replic%e protein% clerly ($e common origin B9C,
%ugge%ting t(t t(e c-ui%ition o) MP% occurre* more
t(n once. Plnt $irl cot protein% re e$en more *i$er-
gent, %(ring )unctionl %imilrity but little or no *etect-
ble %e-uence %imilrity B6C. P(ylogenetic nly%e% o)ten
re$el *i))erent tree topologie% )or in*i$i*ul protein% or
genome %egment% B3C, %upporting mo*ulr e$olution
%trtegy )or plnt $iru%e% B@C.
0ource% o) $rition
,(eoreticlly, ll !"# $iru%e% ($e t(e potentil to
e%tbli%( $ery lrge popultion *i$er%ity, becu%e o) t(eir
error-prone repliction n* %(ort genertion time%. 6ow-
e$er, t(ere i% little relible in)ormtion on polymer%e
)i*elity o) !"# plnt $iru%e%. 7%timtion% m*e )or
%pontneou% muttion rte% o) ,obcco mo%ic $iru% were
not %igni)icntly *i))erent t(n e%timte% )or niml !"#
$iru%e% B9C. ,(e lc' o) in)ormtion on genertion time, or
in*ee* e$en w(t con%titute% genertion )or plnt
$iru% (% m*e %uc( e%timte% *i))icult. 7+perimentl
e$o- lution %tu*ie% u%ing t(ree plnt $iru%e% *emon%trte*
t(t t(e muttion )re-uencie% >)ter un*etermine*
roun*% o) repliction, mo$ement n* negti$e %election?
rec(e* c(rcteri%tic le$el )or ec( (o%t–$iru%
interction t(t w% %tble o$er numerou% p%%ge%
B80,88

C. ,(e con- %en%u% %e-uence% o) t(e $iru%e% were
%tble, e$en w(en %witc(ing to *i))erent (o%t, >i.e. no
po%iti$e %election w% ob%er$e* in t(e%e %tu*ie%?. ,(e%e
%tu*ie% l%o in*icte* correltion between muttion
)re-uency n* $iru% (o%t rnge, %ugge%ting t(t *i$er%e
popultion% con%titute n *$ntge )or !"# plnt
$iru%e%. =n nturl %etting%
plnt% re rrely )oun* in monoculture, % %een in gri-
culturl %etting%. =n%ect )ee*ing i% li'ely to trn%mit
$iru% to $riety o) plnt (o%t% n* (o%t *ptbility coul*
men %ur$i$l )or plnt $iru% in nturl %etting.
4n)ortuntely, %tu*ie% on plnt $iru%e% in nturl %etting%
re lmo%t non-e+i%tent, lt(oug( )ew ($e been con-
*ucte* recently t(t ($e been limite* to loo'ing )or
%peci)ic type% o) $iru%e% B82C.
Arition n* (o%t *pttion cn l%o occur t(roug(
re%%ortment in $iru%e% wit( *i$i*e* genome% n* recom-
bintion. ,(e%e mec(ni%m% cn %er$e to eit(er incre%e
or to limit genetic $rition. 7+perimentl me%urement%
o) plnt !"# $iru% recombintion e$ent% ($e been *one
in only one %y%tem, .rome mo%ic $iru%, w(ere t(e )re-
-uency w% $ery (ig( B83C. =n generl, t(e bromo$iru%e%
%eem to generte little %e-uence $rition B80C, %o recom-
bintion mig(t be n lternti$e mec(ni%m )or
generting popultion *i$er%ity in t(i% genu%.
!ecombintion pper% to be re%pon%ible )or t(e
*pttion o) i%olte% o) Cucumber mo%ic $iru% >CMA? to
l%tromeri B84C n* t(e e$olution o) e+tnt CMA %trin%
e$i*ently occurre* t(roug( bot( recombintion n*
re%%ortment e$ent% B3,89C.
Ienetic *i$er%ity n* popultion %tructure
# recent re$iew on $rition in plnt $iru% popultion%
gi$e% bro* o$er$iew o) genetic *i$er%ity n* popultion
%tructure B86

C. Ot(er notble %tu*ie% inclu*e n nly%i%
o) %trin% o) CMA nturlly occurring in Cli)orni t(t
were ble to o$ercome geneticlly engineere* re%i%tnce
to t(e $iru% B83

C n* %tu*ie% on w(et $iru%e% )rom "ort(
#meric n* ot(er prt% o) t(e worl* t(t %ugge%t trn%-
#tlntic mo$ement o) %ome o) t(e%e $iru%e% in recent
yer% B8@C. #n nly%i% o) numerou% 0ugrcne yellow le)
$iru% i%olte% )rom t(e #meric% B89C %upport% pre$iou%
t(eory t(t t(i% $iru% e$ol$e* by intergeneric recombin-
tion between polero$iru% n* luteo$iru% nce%tor% B20C.
O$ercoming (o%t re%i%tnce
Plnt% u%e po%t-trn%criptionl gene %ilencing % mec(-
ni%m to combt $iru%e% B28

C, n* mny !"# plnt
$iru%e% ($e e$ol$e* %trtegie% to circum$ent or %uppre%%
%ilencing o) t(eir !"#. =n %ome c%e% $iru%e% ($e
e$ol$e* new gene%, %uc( % t(e CMA 2b gene, t(t i%
o$erprinte* on t(e $irl !"#-*epen*ent !"# poly-
mer%e gene B22C. =n ot(er c%e%, $iru% gene% ($e
probbly c-uire* **itionl )unction% to counterct
%ilencing, %uc( % t(e 6CPro o) poty$iru%e%, w(ic( l%o
%er$e% % prote%e n* % (elper )or $iru% trn%mi%%ion.
#lt(oug( plet(or o) pper% ($e been publi%(e*
recently bout $iru% in(ibitor% o) gene %ilencing, mo%t
o) t(e%e ($e **re%%e* mec(ni%tic i%%ue% bout %ilenc-
ing, rt(er t(n e$olutionry i%%ue%. Per(p% t(e mo%t
intere%ting re $iru%e% t(t %o )r ($e not been %(own to
contin gene% to %uppre%% %ilencing. 6ow *o t(ey %ur$i$e
t(e (o%t *e)en%e%J
,(e ot(er well-%tu*ie* )orm o) plnt re%i%tnce to $iru%e%
i% in(ibition o) $iru% mo$ement. Mny o) t(e%e e+mple%
in$ol$e (yper%en%iti$e re%pon%e, w(ic( inclu*e% pro-
grmme* cell *et(. 0ome plnt%, %uc( % C(enopo*ium
-uino, %eem to mount %uc( rection to lmo%t ll 'nown
40@ 6o%t–microbe interction%: $iru%e%
plnt $iru%e%, w(ere% ot(er plnt% ($e $ery %peci)ic
re%i%tnce, %uc( % t(e "" genotype tobcco t(t re
re%i%tnt to ,obcco mo%ic $iru%. ,(e%e gene% ($e l%o
not been e+mine* %o muc( )rom $iru% e$olution point
o) $iew % )rom mec(ni%tic point o) $iew, but t(e%e
%(oul* pro$i*e e+cellent %y%tem% )or t(e %tu*y o) (o%t–
$iru% interction% in e$olution.
Airu% e$olution n* %ymbio%i%
0ymbio%i% i% o)ten %%ocite* wit( mutuli%m, but t(t i%
only one type o) %ymbiotic li)e%tyle. ,(e cl%%ic *e)ini-
tion o) %ymbio%i% i% two entitie% li$ing toget(er. .y t(i%
*e)inition $iru%e% re obligte %ymbiont% wit( t(eir plnt
(o%t%. =n nturl in)ection% w(ere mi+ture% o) *i))erent
$iru%e% mig(t be common, $iru%e% my l%o be %ymbiotic
wit( ec( ot(er. 0ymbiont% my be pr%itic, commen%l
or mutuli%tic. ,(e literture on $iru%e% i% e+tremely
bi%e* towr*% pr%itic or pt(ogenic $iru%e%, becu%e
$iru%e% ($e been %tu*ie* only in t(e conte+t o) *i%e%e.
6owe$er, mutuli%tic $iru%e% re )oun* in in%ect% B23C,
n* re l%o $ery li'ely to e+i%t in plnt%. =t i% cler t(t
lrge number o) plnt $iru%e% re t le%t commen%l, n
interction t(t i% u%ully terme* tolernce in t(e plnt
$iru% literture. ,(e role o) %ymbio%i% in $iru% e$olution
(% been lmo%t completely ignore*, but t(e role o) t(e
(o%t plnt in t(e e$olution o) $iru%e% i% clerly importnt,
% i% t(e role o) $iru%e% in t(e e$olution o) t(e (o%t. =n
mi+e* in)ection%, $iru%e% ($e t(e opportunity to pro$i*e
e+ten*e* )unction in mutuli%tic reltion%(ip, n* p(y-
logenetic nly%e% clerly *emon%trte t(t t le%t %ome
$iru% group% ($e e$ol$e* by recombining t(eir )unc-
tionl gene% wit( $iru%e% )rom *i%tnt relti$e%. =n recent
!e)erence% n* recommen*e* re*ing
Pper% o) prticulr intere%t, publi%(e* wit(in t(e nnul perio* o)
re$iew, ($e been (ig(lig(te* %:

o) %pecil intere%t

o) out%tn*ing intere%t
8. !oo%%inc' M&: Cucumber mo%ic $iru%, mo*el )or !"# $iru%
e$olution. Mol Plnt Pt(ol 2008, 2:99-63.
2. 6rper I, 6ull !, <oc'(rt ., Ol%Eew%'i ": Airl %e-uence%
integrte* into plnt genome%. #nnu !e$ P(ytopt(ol 2002,
40:889-836.
,(i% pper *e%cribe% t(e recently *i%co$ere* prretro$iru%e% t(t re
integrte* in mny plnt genome%, wit( n emp(%i% on t(o%e t(t cn
pro*uce epi%oml in)ection%.
3. Milne !I, MrEc(i C: Crypto$iru%e% >Prtiti$iri*e?. =n
7ncyclope*i o) Airology. 7*ite* by Keb%ter !I, Irno)) #:
#c*emic Pre%%D 8999, $ol 8:382-389.
4. <uc% K&, .ouc(eL -Pillon 0, &c'%on /P, "guyen <, .'er
<, /ing ., 6'e 0: 0electi$e tr))ic'ing o) 2"O,,7/8
(omeo*omin protein n* it% m!"# t(roug( pl%mo*e%mt.
0cience 8999, 230:89@0-89@3.
9. Melc(er 4: ,(e F302G %uper)mily o) $irl mo$ement protein%.
& Ien Airol 2000, @8:293-266.
6. Cllwy #, Iie%mn-Coo'meyer /, Iilloc' 7,, 0it ,<, <ommel 0#:
,(e multi)unctionl cp%i* protein% o) plnt !"# $iru%e%.
#nnu !e$ P(ytopt(ol 2008, 39:489-460.
3. !oo%%inc' M&: 7$olutionry (i%tory o) Cucumber mo%ic $iru%
% *e*uce* by p(ylogenetic nly%e%. & Airol 2002,
36:33@2-33@3.
@. Iibb% #, 2ee%e P2: =n %erc( o) t(e origin o) $irl gene%. =n
Moleculr .%i% o) Airu% 7$olution. 7*ite* by Iibb% #&, Cli%(er C6,
IrcML-#renl 1. Cmbri*ge 4ni$er%ity Pre%%D 8999:33-90.
9. Mlpic &M, 1rile #, Moreno =, Obie% C=, /r'e &K, IrcML-
#renl 1: ,(e rte n* c(rcter o) %pontneou% muttion% in
n !"# $iru%. Ienetic% 2002, 862:8909-8988.
80. 0c(nei*er K<, !oo%%inc' M&: 7$olutionrily relte* %in*bi%-li'e
plnt $iru%e% mintin *i))erent le$el% o) popultion *i$er%ity in
common (o%t. & Airol 2000, 34:3830-3834.
yer%, t(e role o) %ymbio%i% in t(e e$olution o) li)e on
7rt( (% become incre%ingly pprent, n* u%ing
88.

0c(nei*er K<, !oo%%inc' M&: Ienetic *i$er%ity in !"# $irl
-u%i%pecie% i% controlle* by (o%t–$iru% interction%.
& Airol 2008, 39:6966-6938.
$iru%e% % mo*el%, w(ere e$olutionry c(nge% cn be
re*ily me%ure* in % little % two wee'%, mig(t llow
more importnt -ue%tion% bout t(e role o) %ymbio%i% in
e$olution to be re%ol$e*.
Conclu%ion%
Plnt $iru%e% *i))er )rom niml $iru%e% in %igni)icnt
wy% t(t mu%t be con%i*ere* w(en %tu*ying t(eir e$olu-
tion. 6owe$er, p(ylogenetic nly%e% %ugge%t mny plnt
n* niml $iru%e% %(re common nce%tor. 6ence,
be%i*e% t(e importnce to griculture, plnt $iru%e% cn
be u%e* % mo*el% )or un*er%tn*ing b%ic mec(ni%m%
o) e$olution. !ecent popultion %tu*ie% o) plnt $iru%e%
($e re$ele* t(t t(eir le$el% o) $rition re *epen*ent
on $iru%–(o%t interction%. ,(i% re)lect% t(e %ymbiotic
reltion%(ip between $iru%e% n* t(eir (o%t%. #% more
*etil% bout !"# %ilencing, t(e mHor mec(ni%m )or
,(i% pper *emon%trte% t(t muttion )re-uencie% )or *i))erent $iru%e%
e%tbli%( %peci)ic le$el t(t i% n intrin%ic property o) (o%t–$iru% inter-
ction%, by %witc(ing $iru% popultion% between (ig( muttion )re-uency
n* low muttion )re-uency (o%t%.
82. Morn &, $n!iH%wiH' ., ,rice$%'i A, 2itHim 7K, Mc'enEie #M,
Iibb% #&: Poty$iru%e%, no$el n* 'nown, in culti$te* n* wil*
%pecie% o) t(e )mily #picee in #u%trli. #rc( Airol 2002,
843:8@99-8@63.
83. .ruyere #, Kntrob M, 1l%in%'i 0, /Einott #, .uHr%'i &&:
1re-uent (omologou% recombintion e$ent% between
molecule% o) one !"# component in multiprtite !"# $iru%.
& Airol 2000, 34:4284-4289.
84. C(en N-2, Iol*bc( !, Prin% M: =nter- n* intrmoleculr
recombintion% in t(e Cucumber mo%ic $iru% genome
relte* to *pttion to l%troemeri. & Airol 2002,
36:4889-4824.
89. !oo%%inc' M&, O(ng <, 6ellwl* 2-6: !errngement% in t(e 9
0
nontrn%lte* region n* p(ylogenetic nly%e% o) cucumber
mo%ic $iru% !"# 3 in*icte r*il e$olution o) t(ree
%ubgroup%. & Airol 8999, 33:6392-639@.
plnt *e)en%e gin%t $iru%e%, re un$eile*, t(e nee* )or
better un*er%tn*ing o) plnt $iru% e$olution n* t(e
86.

IrcML-#renl 1, 1rile #, Mlpic &M: Aribility n* genetic
%tructure o) plnt $iru% popultion%. #nnu !e$ P(ytopt(ol 2008,
39:893-8@6.
bility o) $iru%e% to o$ercome (o%t *e)en%e% become%
ob$iou%. =n **ition, un*er%tn*ing mutuli%tic $iru%e%
,(i% pper pro$i*e% t(oroug( re$iew o) popultion %tu*ie% in plnt
$iru%e% n* (ig(lig(t% %ome o) t(e current contro$er%ie% in t(e )iel*.
my (elp u% to un*er%tn* (ow t(e rre $iru% become%
pt(ogen.
83.

<in 6-P, !ubio <, 0myt(e #, &imineE M, 1l' .K: Ienetic *i$er%ity
n* biologicl $rition mong Cli)orni i%olte% o) Cucumber
mo%ic $iru%. & Ien Airol 2003, @4:249-29@.
Plnt !"# $iru% e$olution !oo%%inc' 4
www.curre n t-opinion.com Current Opinion in Microbiology 2003, 6:406–409
,(i% pper report% compre(en%i$e )iel* %tu*y o) %trin% o) Cucumber
mo%ic $iru% in Cli)orni, inclu*ing %ome t(t re ble to o$ercome t(e
engineere* re%i%tnce to t(e $iru% t(t (% been *eploye* in )iel*% in
Cli)orni.
8@. !ben%tein 1, 0ei)er% /<, 0c(ubert &, 1renc( !, 0tenger /C:
28.

between luteo$irl n* polero$irl nce%tor%. Airology 2000,
269:896-838.
Mlot%(w 0, Aoinnet O, Mette M1, MtE'e M, Auc(eret 6, /ing
0K, Pru%% I, Ance A.: !"# %ilencing n* t(e mobile %ilencing
%ignl. Plnt Cell 2002, 84>0uppl 8?:02@9-0308.
P(ylogenetic reltion%(ip%, %trin *i$er%ity n* biogeogrp(y
o) tritimo$iru%e%. & Ien Airol 2002, @3:@99-906.
89. Moonn 1, Mir'o$ ,7: #nly%e% o) genotypic *i$er%ity mong
"ort(, 0out(, n* Centrl #mericn i%olte% o) 0ugrcne
yellow
le) $iru%: 7$i*ence )or Colombin origin% n* )or
intr%peci)ic %ptil p(ylogenetic $rition. & Airol 2002,
36:8339-834@.
20. Moonn 1, Molin &, Mir'o$ ,7: 0ugrcne yellow le) $iru%:
n emerging $iru% t(t (% e$ol$e* by recombintion
,(i% re$iew pper gi$e% t(oroug( o$er$iew o) po%t-trn%criptionl gene-
%ilencing n* t(e $iru% gene% t(t ($e e$ol$e* to o$ercome t(i% plnt
*e)en%e mec(ni%m.
22. /ing 0-K, #n*er%on .&, 6%e 6!, 0ymon% !6: "ew o$erlpping
gene enco*e* by t(e cucumber mo%ic $iru% genome.
Airology 8994, 89@:993-608.
23. ,urnbull M, Kebb .: Per%pecti$e% on poly*n$iru% origin% n*
e$olution. #*$ Airu% !e% 2002, 9@:203-294.

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