'J
sM 5. 1J 7 Izck
CITA
41,±411310tElfit'l
(IsR) o)(t=XL,
R.4
*, Come Pieterse*, Leendert C. Van Loon*
Shu Hase, Come Pieterse, and Leendert C. Van Loon
Mechanisms of Rhizobacteria-Mediated Induced Systemic Resistance
Abstract
Some of non-pathogenic rhizosphere bacteria reduce disease by activating a resistance
mechanism in the plant called rhizobacteria-mediated induced systemic resistance (ISR).
Rhizobacteria-mediated ISR resembles classic pathogen-induced systemic acquired resistance
(SAR) in that both types of induced resistance render uninfected plant parts more resistant
towards a broad spectrum of plant pathogens. In contrast to SAR, ISR induced by
Pseudomonas fluorescens WCS417r functions independently of salicylic acid accumulation
and pathogenesis-related gene activation. Mutant analyses showed that this ISR follows a
novel signalling pathway in which components from the plant hormones jasmonic acid (JA)
and ethylene response are successively engaged to trigger a defensive state that, like SAR, is
controlled by the regulatory factor NPR1. To investigate the role of JA and ethylene in ISR,
their production was monitored in ISR-expressing plants. Neither local nor systemic levels of
JA and ethylene production changed upon induction of ISR. Therefore, we postulate that ISR
is mediated via an increase in the plant's sensitivity to JA and ethylene. Interestingly, ISRexpressing plants show an increase in ACC-oxidase activity, providing a greater potential to
produce ethylene after pathogen infection. In addition, ISR is associated with the potentiation of
specific JA-inducible genes, resulting in an enhanced level of their expression after pathogen
infection. These results suggest that ISR-expressing plants are primed to express ethylene- and
JA-dependent defenses more efficiently upon pathogen infection.
Key words: Pseudomonas fluorescence, Arabidopsis, defence signalling, ethylene, jasmonic
acid, salicylic acid
41 t.;66 I:
ztio4MMAIPP-5-1J7/Mr:4AALLMtUsMEI*01AV(7_1-z
* Section Phytopathology, Faculty of Biology, Utrecht University, Utrecht, The Netherlands
** 310LX
PAM* ffgAf=1- Graduate School of Agricultural Science, Tohoku
University, 981-8555, Sendai, Japan.
15
#111fittrA41-6. :_otaliftl,14113144.tritft (IsR)
7,
-1.,'-ct9-( )1/7.
a,
<
I
U c3
SARl
4i'ltiff-glitit(SAR)LXNMaitrCL6b1,
4-1.-C-6
Tti 6 Z71
M6±."-CNI*Mti).
LCS U
)
5- U
:7--XL
'iJ7
U
1.
)-
I; t:,
U
`jR9 5-0 771grA-
bibb\
Lu, iiA4tErriftoVrzts)(t.7-XIA
Lts6t$1441V-ifto):>9'±)1/13tVkil6
ISRO
5--1)
.gt34.< ofiltfiaAJA14:5(1.1.-COAknflzi) tu-C1/16. ISR
t/N tt.6
Z6.
*att., rAm,
7 ODPseudomonas fluorescens WCS417W 41-4z Lts 6
LV,P111-Lt.::
L7.41.1-C49ffi-D- C
s
7b141.LtS41-44titriiit(ISR)
tttft11. AirWo)13z*ffiGq6t--,:673i-J_I,)<-Db\01314ftolUIMIN{MA_ Ti/N6.
Mtct <R9Yffii.C95 (54-1.--Cu)633141t0IM&VI. A3,EL tts5Mgf*M-Oft
-ritttiE 116 t ---es -0)**.tt404Pt131:fBiZbiTrAU: 0AIRWoftffit4i'ltf'41-1V-ift(SAR)LtAti--C.t3
5(4-1.-CtAtrin4:-.ts6.
co(
"fsettLMJC*0-A11.(7-,--Ett-D-q---C4M-tt-ct/N6
(Ross,1961),
(Hammerschmidt and Kuc, 1995, Ryals et al., 1996; Sticher et al., 1997 ; Hammerschmidt,
1999).
AWARE. tilAffi Izt,12.1.-C1/6
Ott'',
:-/-5-10
Ni/5-ij 7orla1:41,
7 A- 7 Vii-q-Ur:_r A- .> 00112iAbriE ttNO3-}t6L
±4to
-c-±4,14-;41.'t
MAL 1.,--cillt®ARVZiE-d-6 Lb16(Bakker et al.,
Migf Lilt-MIA
U 7 id, 4:11Xffi tais Liettolkts Ea)
Llz,
1991). IP:, Al*M
I_EffMgM4-6AJ#1*(DiMM1110.110)60 -DI 0
V/I5---IJ 7 Lift 0411-CofflEffifiolZA. am-
*LoDittOoftdircatIts<,
fikiieti*{*t:i314
grAft(IsR) lif Idtt.
1.,T,
77E
*
1998). *, 77 E F 7°:.7
U 7 LAP:
,
;t14,-c- to 6.
-f 7°0#011111,141114
3f-f .>, /R,D.
r, 11
7.
o4 altfir,7_,31,N--c-citr-c-t,N6 (Van Loon et al.,
11.
'J/75IJ 7
Pseudomonas.fluorescens WCS417r
Dz---5111J-N1- 6 z: LT. AJA-15-"-I.J 7 0) P. syringae pv. tomato DC3000 (Pst
L Xanthomonas campestris pv. amoracia, MOTU, Fusarium oxysporum f. sp.
bib -"D C rz
4tgvi ft 774raphani
Peronospore parasitica
t
(Pieterse et al., 1996; Van Wees et al., 1997; J. Ton, unpublished results). (It'll; OAR.
DC3000)
t.:5(1---4- 6 taiiitta. mmotingLAW4KoiMoK.Mlz..
11/*It0)7 E rif/A
=X
T- 1/ '117.-C'rifiai: flgtfit
ISR
L
TIT
1,-:
Lt
-csifffil- 6 LbiT
1LS -0M14,tt
(1:1
ISR OD:7 Yt11/ii.tfni
2.
2-1.
-9-1)
Ltkr-4- Ltst,):/Yt)lpfilfhlIM
*EXiNt'i0)AiRf*k7.ct 6 SAR ODIVA
16
`9-1.) -)1/fOtliNlin L (Malamy et al.,1990;
Métraux et al., 1990),
-cIrs,v4art<337.->/witi
(PR) blt&fitl6
Ca6(V an Loon, 1997; Ward et al.,1991)0 11100)-it '')I/FMJ1.17.1031174f1=Miti.
i±
(nahG)
U .-)1/fit-M:f-r-eV-s< Lk NahG XRCtMettil, SAR
7its14 tur. PR
IEL1 Z.: Lffi SAR 0:2 ,49-)IpE311,1ii-1)
t.
fgiziA41-6 LI' LON i;b4:1I171t(Gaffney et al.,1993)0 7 E
SAR 17_ 6 18&-C-9- U '-)1/fg41V-A L PR MAIL 416 (uknes et al., 1993; Cameron
et al., 1994; Mauch-Mani and Slusarenko,1994)0 NahG )1MC4A1*J1E1(/ LAM ffi 6 ,
7 7 E Fif/A--et SAR or):>Y9-)1/1-11,1-9-1J -)1/M ;:c1A4-L-cti6 LON Gffi
tz.*4-11 (Lawton et al., 1995). lit, "#' I) ..)1/61ce
tctffi 1
JZCS
Iti.A14 qt.
anti
--C
SAR
t PR ?Mitt 41ts
41 NPR1
I
nprl
tar4.1.k.(Cao, et
al.,1994).
SAR
,
)1/fgoVAJ.
WCS417r
L,t77 E Fl>X0r) ISR a, "9-1J ti
!t0 cJZC
PR ot-&-tt1LV#1-3tsti.
CIC* 41, Pst DC3000
j U '11404:41{3k4- Lai/
2-2.
i4:At_f-N
ZL.
WCS417r
Lit NahG JFW
F,Yt/l/fita,
RIL1J
ISR
/to (Pieterse et al., 1996 ; Van Wees et al., 1997).
Lblt)ffi
VA, A ,.2fg, I3 1/ >Pi;
SAR 0:-/Y9--)kriClialit424 L.1-I/./4:7.41f-A4Utottio
I>t
ISR (d. :7"-,A7FOLIV'Azg-s.?
E F V'f/
S16R3-1-, tsGZ.XV: NPR1 (.111K4 Utz (Pieterse, et al., 1998). 1-tsbt , A, A
.>&14:_g:c
jur1-1
etr1-1 5tia*, tsGZX
npr1-1 OR,wa.
WCS417r
IC#J Pst DC3000 I1-61:1MWCS417r
V-N1,1-c7
fiV,314.-etsffi-D tt.
:Y.)-)1/,{"itoffI4in6L-t951.--:)c)1.77-rA
fg jar1-1, etr1-1 L npr1-1 vjcal*i,:ttiv Utz:
,
olf.A4 ttittf-Efi
--C---tsbN-Dt.:7 51,
>0111.1ffilK-c; 6 1-7
o
R.> 1 t)1/.7
G
:71,- 1-(ACC)Alf-N1-
L jar1-1 stinWillEtfittfisi4
5mwittgrmst,1314---Ctczffi-D /to
L. R6
etr1-1
nprl
T, WCS417r 4,:ct-D-Cfg4t16 ISR 0):>Yt)14-441, 11101-,::;t
6
SAR PM: NPR1
k=ct.--D -CFM-4-6 Mii:{1K4 L.
fik*---4- 6 ffffti
E'D
6
ttk (El 1 ; Pieterse, et al., 1998). NPR1 as
SAR 0)Y9-)1/11.tr04--c11.--0-Fir-e PR (DiSitiL
< 751, ISR 0):Yt)1/1-3*
Lit/
*Weil PR
i-81111LLtsti(Cao et al.,1994; Pieterse et al., 1998). `DI
111--T-61/ 41, Ik110) ISR r41411-1T-oftiMbi,
UT. NPR1 bN6ntsX1"6.4(1--Ct
Aj:341.6.
2-3.
#
ISR L
SAR 0)77 Yt/l/iit ariti
'...)141a4d,
L Litty-q---c4k6 L,
EL)1,7: Ea-ACV-T-01-6 ODffi
-tt.-E-41.±..b1.0)404i:{1k4
te
6 (Reymond and Farmer,
L SAR1,1 Lt 1 NPR1 ct "D -CAM t1.6
>RIATI0MgS
1998; Pieterse and Van Loon, 1999)0 ISR
SAR Rtii*
$1.1"-i- 6 Li'
L 51
(7_
>F0g;i4i-.:{A4- ® ISR Lit')
fta-Y0) SAR 751
T, Van Wees et al., (2000)41A
5 kin 751 <0
17
:>Y.)--)1440-)
TJJS
DA
Ttst-Dt
1:--31,)-Cf1M Litto
I-
41-6 WCS417r
ISR
avrRpt2Al Pst DC3000
SAR
C7-911fN1,/tL:._, -Z-07
L-0
tftfiftbilk
E
tiA4T ts ti) NahG JRWC14*. A (,)11 ISR
etrl, jarl
1$S WCS417r L Pst DC3000 (avrRpt2)
ttfitAttkl§ tsi-3/sM---Dtt. 6 t:, SAR
PR-1 OR
1JW1, ISR SAR 19-)Pi5tWl.,'"CL)Ztittti SAR OW-)-4iL-C1.)ZtilltL0)
SAR
)7
1tt,
rrAitZZbitSffi-D
NPR1
tzlit41-6
.Yj-)1/{3t1,1,
SAR L ISR
Lts< 111,1141kii-TY±)1/bifl-DZ LA-A_ Gtt.Z.
IJ
`1)
5- 1J 7 0) P.
aeruginosa
7NSK2 scb, il1-40'91:qt 'J
)1A
.18#1.13EIN
-ttz:
P3 **All, fRO-AffiT-9- 1J --)litikctgl-Z z: LT, ettz-it1J9-)1/
fM:fik41.,tz_-:>Y±11/1-3tVOt-q-Zz.: Lbil-Dffi-D-Cti)Z(De Meyer et al.,1999a,b;
Maurhofer et al., 1998). WCS417r L:14160 'JR 7 5---U 7
1st 1,-C±4(:).81111ti ct Nti4Affilt fttr-4-Z
L;?,_60
P. aeruginosa
1J 7
It1
tXM4A)g{*
I
4.
tA
1jarl
.2fiDtS
4.
!IF
# 9 ../Lftt
1etrl
,2
NPR1
IMMIRMItN
nprl
PR37
ISR
VI 1
3.
NahG
SAR
ISR Mitt 9'±)1/firftiTi
(Pieterse et al.,1998
9)
c
0,
ISR &ZODINA
3-1.
ISR
SAR
--4-et-cus u
SAR 03-}-T-7t --(CtS-D-Cl/)60
az
T.
lt
-\- PR
-,9) PR tl,
Ef'1:-/
WCS417r
-)1/1fOldgfAli1 PR tikitiLli/V.). L:ttITin[1641-C(/)6M4P
t
I
tilt&
i7-igf-V Lit
05-24 7 7 l/.2-t/l/A
IM411.-TOMIYJAciE
----11:4170fiLL-MAizt
ft41M-141
tsffi--Dtt. (Van Wees et al., 1999a)0
E1. WCS417r
E 1.7*.bNi=31/fT41.,/-z: cDNA
18
>YAWL.
11-1--t-s 6 Z.)
A'Ra) 2 'TcY)1/-M%-iii<fhii'plfi1.-:-D--CtftfM'Ar.
RUN:DO- Glitsffi-D t= (Van Wees et al., 1999b)0 SAR a
37
WCS417r
ct
L1,1%1110471.: , ISR Mg; Tr: 111
'111
37
Ltitst,).
>fit Li.-1,.71-:.3(44-6WrooDS1.-It
3-2.
ØI>COU witiv
, fit
linPaZ AliA
41.-"C tO 6 (De Laat and van Loon, 1982; Gundlach et al., 1992). Af/y1--)t,,-}-Tq1 , A
toirclit.trzi:qk'
77-1,
r1:2A1,1, Pst DC3000 t:Int./TIA.
ft
(Boller,1991;
g
_1.4 Lit 7 7 E
Pieterse, et al.,1998; Van Wees et al., 1999a)0
WCS417r
iF/A
1/ >fiA41toRVOMM.11
>t0b5
itT (Lox], Lox2, Atvsp, Pdf1.2, Hel, ChiB, and Pal) 0) EtItattiLtrt
(Van Wees et al., 1999a). :101- Lffi
WCS417r 7V7 7 E
Ltst/4-.6 5 LtftV:111-,:..
9410117-:)%t
ai-12 625 Gtit-sffi
> rek 4111 t 1,ttbis
ffi r,:VAE-4 :A ts
ty
E >6.1ceAb.i. 1/
tt( Pieterse, et al., 2000). ISR a,
ct 0
t:{1k41.,-c
< ts-D
::41.1730*)1/,'A:_91-1--Wialt
cAllto
R
3-3.
:it
F)A,A>Filce1-:_cLD--CgA41-L6itf-ftiRoDt5"->,-t)1/
7 E F I: optU:ZJI
1-, 1,2:4041-64g-c11, WCS417r
::)-\,>titLx.fl7>o)lantsZfLatst,),,
/Sr
1_17
>ot.A41#5rMig1*ffirzVt..L.L1z, --a)tfifoitt, J
*16.
14
---C
t
tbtao
-C
WCS417r
--.0)ttilttb1:;-\-2
1,< az1 -6
Lbim
-it.r7YT,L\tIgifttl/413,>1-1=1)1/LL
7 EF i-E/A
WCS417r
Pst DC3000
(Atvsp, Pdf1.2, Lox2
Pall) L.
>
>R4-314tt
>riAattoi-tf-T- (Hel ChiB) oRfRiatait)z- Lit (Van Wees et al., 1999a). --12)
WCS417r
fR(:_ttf-g kVA OV)13 >1- t=1
MT,
1/ .2 ''tOft L ttm--e
)l/taltrj:.tLiCAL) Atvsp 0ftNiA-it
614ft
Li ISR "Ca,
lafftglo)71i5=-.2:-/t/1/751MJC*013tVI:INA.--CIAI-D-CLItiVtItt.
c
'it
3-4.
.1.n,:/t*CD)ii5---,>t)1/
A":S:kittt-C11, .1;fl/:/id, s-7-5-2J .)1/?(
.>ffir6 ACC r''''AtlIA0fittat:_.
ct J ACC (::12Ati, '-1-11)1W)-C-- ACC FOILtO*omizt1
(Kende,1993; Kende and Zeevaart, 1997; Theologis,1992)0
7 13 13
f/A.t6 ti14/-
1=1:/A0MitA.-41-A1,q41)116,'*1./ttt.hlt(il, ACC 12-1ANIAtsr3Z1k: ACC Mt`
(De Laat and Van Loon,1982)0 lArTioff
fLEiMblikttfLllm..- 1/ >abqM)iir--4L. SAR
AT, SAR W%C,Tr:l.k.37/I3C1, ACC
19
ote0/1DAiz ACC
tc.
.1.1n1:7_VV1.1t.14frizi1-c,
(De Laat and Van Loon,1983)0 'DI 19 SAR
i,n..7thta7)iA5-D
AT'id, ACC
WCS417r
11:
l/ A:1_111-6 ACC fitintAitithiAc< ts-D -cwt.
EgUtz.-77EFIA11, it±ii1A41.41a: ACC Vrt-tn1-.7:4A..6L,
>17)1,
77E F 7°:/A1,7_. ACC
(Pieterse, et al., 2000). ISR );'6 -tA
-E-
t
-q-A_/-z-_tA
T 20^-50% E1A\-D t
tt 7 -7 E F
, ACC 7" .r...1,,>1:-0411--4-6 ACC FOILFilVtitbiai<ts-D-coft. 77Er
1_,
WCS417r
7°:2
ViZ9,11,1Nt.ittfc..=41eidt_E.SVII.114T0)11/,'/IACI'M
iligts-ItlElfltsli)(Pieterse, et al., 2000)0 Lt:_bi-) Ts WCS417r f.Rtz:11,4 L tz7 E
F.1:',A--c ACC AktftMittiki-A<ts-D--co6L:
1,>:;t0f11164fi
ts--)--0,6 Lrqd,-c-to6L4-
Glitto
AidoW5-re,
fNUt-z77E
A_
1,
>
-r 7'0 Pst DC3000(avrRpt2)
WCS417r 595
1/>:710fiLftL
.-/I,E1)atttz Pst
DC3000(avrRpt2)VOR Lk:War
x. I/ >E47514g1:r-Cil
bibb''"D
tt(S. Hase, unpublished result). Alternaria brassicicola 0).t 6 l/A id, 7 7E F 1
AiZIN10-11.1/ >
-17AE>R0)-ViVZt.,
:2E0/fiklz1
40)ta.---dt
1-6(Penninckx et al.,1996; 1998). ISR &fit
>tA0)1-Z5->f/t)1/birAti)::
AVZL,
itiett-C1. I/
Aigi*Ogt*fe.iitttLC:,
1-A4011-A4tAllift.ti9AVihtzR
L LIMID-D-c-66)-eidtsii)ffiLA. ttrc.
111
1319 01:
'-ii1W1t,a):
LV1,
t )1/{-itfil5alliV:13414 6,ffrito fit ido)iLkINI::
let1113M-4-6RAto-)37-1'11:1A4't,-c
M.1111L-4-6
LbiT 6 L V 5 Z71
"C"
--ChM
SItsIM'fIlaZo-)F,Y/-)1/{
6 (Bostock,1999; Dong,1998; Glazebrook,
1999; Maleck and Dietrich,1999; Mauch-Mani and Métraux, 1998; Pieterse and Van
Loon,1999; Reymond and Farmer,1998)0 *fit
I, It IJ
I) 7 Pseudomonas
fluorescens WCS417r Zf-g L it 77 El-t 7°-:> id,
1J ')1/f0 Vs:fikr4
SAR L 11A
f;Atczlo,
tiiltiz
0)FrAti:fik4L7-z-AllitiliA41.tt.
,.)1/ftkf-ik4otgrfiftitsi'-41-6 ,)-,7-- I) 7 tA-iffi--D --c.V-zo -it ..-)1/ftt
fA4L A,
>ffk
1/ >P6,4 r,:f1K41,
A/fit MS*
LLTIMMLUAVIVIA-41.k.:z.: Lb) 6, Ats6 F,Yt)1/fitigi4-4--6
1J 7 oDMA Vritti
L-c-CL:Currtaf,
1-11-fENI-614tigit
":!..: Lit.
040fild 6
< 0)f100)JC*1:tA
LA'A.
ISR
IC:"D
i/1T, aidoriff5t-chb\--D-c-
V-k,,E>FOLi-1,>ki141:7_AP:f*orAVid-t.:1141-Wts.R,V1
5a:L--c6c. Tabt, ISR --c11,
,X2rMzoto-CteliN
>:>A7/1/7)i, Ai< ts-D-ct,Itto
20
a:.
2 *9
t
s>fgL1:. 1/>i:.:{k4Uts:MP&ZblAIRP*01AIRCitt--,:L
oftRid,
.ff0A0))4111<li:Rf)11-6:_LLIIMU-5--C6 (1212). L1. MINIKZ0
t
./:;40101141Liltsin'Lz VAE91--6-e6
'n6
-k,A>fgLi....-1,.>011111-)
Li:
l/
MOIN1411f-f-OftiRbi.
1-tct i; id, a:
VAibl ISR
MOPRZ0VJWili.:1341.6
L7)1 ISR
rj...fgALT-4-
6#41*Mt/e5tara0-)ZiL`DT60
Pseudomonas fluorescens WCS417r
4
VA-A>f0.M.L/>Z417_
fiK4-0:-/YtA/A
>fgaiVit
111--TIVA®
.4Z
>
7J-Z
(ACC :-..-ILAMM-It)
)1,
NPR1fA40)
itrk
:iY1-11,fat
1
xJ-1,
>fittiPSit
05.1{109,
M Wit
03.1f=f-R41.?
4.
MfA1MZ
RI 2
ISR IS-OtTor).M.1/
(Pieterse,et al, 2000
L fis t
.mot)
>K0115141i:r4{haR
AKI5ZIL&1)i,--:/-z O *iLk2-*AiiUM-tt4±,:t 0 'ft
RE 1, TVA* L±.(111-0
fflA
ti4-z:tz-2
ult.
MI3Za
Bakker, P.A.H.M., Van Peer, R. and Schippers, B. (1991). Suppression of soil-borne plant
pathogens by fluorescent Pseudomonads: mechanisms and prospects. In Biotic Interactions
and Soil-Borne Disease (Beemster A.B.R. et al., eds). pp. 217-230. Elsevier Scientific
Publishers, Amsterdam.
21
Boller T. (1991). Ethylene in pathogenesis and disease resistance. In The Plant Hormone
Ethylene. (Mattoo, A.K. and Suttle, J.D., eds). pp. 293-314. CRC Press. Boca Raton.
Bostock, R.M. (1999). Signal conflicts and synergies in induced resistance to multiple
attackers. Physiol. Mol. Plant Pathol. 55: 99-109.
Cameron, R.K., Dixon R.A. and Lamb, C.J. (1994). Biologically induced systemic acquired
resistance in Arabidopsis thaliana. Plant J. 5: 715-725.
Cao, H., Bowling, S.A., Gordon, A.S. and Dong, X. (1994). Characterization of Arabidopsis
mutant that is non-responsive to inducers of systemic acquired resistance. Plant Cell 6:
1583-1592.
De Laat, A.M.M. and Van Loon, L.C. (1982). Regulation of ethylene biosynthesis in virusinfected tobacco leaves. II. Time course of levels of intermediates and in vivo conversion
rates. Plant Physiol. 69: 240-245.
De Laat A.M.M. and Van Loon L.C. (1983). The relationship between stimulated ethylene
production and symptom expression in virus-infected tobacco leaves. Physiological Plant
Pathology 22: 261-273.
De Meyer, G., Audenaert, K. and Höfte, M. (1999a). Pseudomonas aeruginosa 7NSK2induced systemic resistance in tobacco depends on in planta salicylic acid accumulation but
is not associated with PRla expression. Eur. J. Plant Pathol. 105:513-517.
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