the phytotoxic lipodepsipeptide syringopeptin 25a from pseudomonas syringae pv syringae forms ion...

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The Phytotoxic Lipodepsipeptide Syringopeptin 25A from Pseudomonas syringae pv syringae Forms Ion Channels in Sugar Beet Vacuoles A. Carpaneto 1 , M. Dalla Serra 2 , G. Menestrina 2 , V. Fogliano 3 , F. Gambale 1 1 CNR, Istituto di Bio®sica, Via de Marini 6, 16149 Genova, Italy 2 ITC-CNR IBF, Centro di Fisica degli Stati Aggregati, 38050 Povo Trento), Italy 3 Dipartimento di Scienza degli Alimenti, UniversitaÁ di Napoli Federico II, 80138 Napoli, Italy Received: 15 February 2002/Revised: 26 April 2002 Abstract. Syringopeptin 25A SP 25 A) belongs to a family of cyclic lipodepsipeptides LDPs) produced by the gram-negative bacterium Pseudomonas syringae,a phytopathogenic organism that aects several plants of agronomic interest. LDPs increase the permeability of plasma and, possibly, intracellular membranes in plant cells. Consistently, SP 25 A forms ion channels in planar lipid bilayers and other model membranes. Here we used sugar beet tonoplasts as a new biological model system to study toxin action. When applied to the vacuoles by a fast perfusion procedure, SP 25 A in- creases membrane permeability by forming discrete ion channels even at low applied potentials. The SP 25 A channel displays anion selectivity with a Cl /K + permeability ratio of 6.7 1.3) and has intrinsic rec- ti®cation properties that derive from a dierent chan- nel conductance at negative and positive voltages, presumably owing to an asymmetric distribution of ®xed charges on the pore. Substitution of chloride with dierent anions reveals the following selectivity se- quence NO 3 Cl >F >gluconate , suggesting that the permeation pore is ®lled with water. The properties of the SP 25 A channels in vacuolar mem- branes are similar to those observed in planar lipid membranes prepared with asolectin. This work pro- vides a direct demonstration of toxin eects on a native plant membrane, extending to a biological system previous results obtained on arti®cial planar lipid membranes. Key words: Ion channels Ð Patch clamp Ð Anion selectivity Introduction Syringopeptin 25A SP 25 A) is a lipodepsipeptide LDP) produced by the plant pathogen Pseudomonas syringae pv. syringae Bradbury, 1986; Ballio et al., 1991). It is composed of two parts see Fig. 1D): a peptide moiety of 25 amino acids with a cyclic ring of 8 amino acids at the C-terminus and a long un- branched 3-hydroxy fatty acid chain attached at the C-terminus of the peptide chain. SP 25 A is a basic molecule since the cyclic ring contains two positively charged residues 2,4-diaminobutanoic acid) Ballio et al., 1991; Isogai et al., 1995). The three-dimen- sional structure of SP 25 A in aqueous solution, ob- tained by the interpretation of its two-dimensional NMR spectra Ballio et al., 1995), is characterized by three structural regions: a loop including residues from Pro2 to Val6, a helicoidal zone close to a left- handed alpha helix) including residues from Ala8 to Ala15, and a large lactone ring including residues from Thr18 to Tyr25. The type of ring conformation is the same found in two other bioactive lipodepsi- nonapeptides, the white line-inducing principle WLIP) produced by P. reactans Mortishire-Smith et al., 1991; Han et al., 1992) and siringotoxin pro- duced by P. syringae pv. syringae Ballio et al., 1990), and resembles the seam of a tennis ball. Its marked phytotoxic activity Iacobellis et al., 1992; Di Gior- gio, Camoni & Ballio, 1994; Di Giorgio et al., 1996a; 1996b) indicates that SP 25 A may give a signi®cant contribution to the virulence activity of P. syringae, Abbreviations: SP 25 A: syringopeptin 25A; SRE: syringomycin E; LDP: lipodepsipeptide; PLM: planar lipid membranes; SV: slow vacuolar channel); PC: phosphatidylcholine; PE: phosphatidyleth- anolamine; PS: phosphatidylserine; LJP: liquid junction potential; R a : access resistance; EDTA: ethylenediaminetetraacetic acid. J. Membrane Biol. 188, 237±248 2002) DOI: 10.1007/s00232-001-0187-x Correspondence to: A. Carpaneto, email: [email protected]

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&414+<4.Q !G A4R6,26> "FF"S&4<+)4.Q "8 DL6+= "FF"

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L46M42R+=+*> 62*+- -T 8X_ ` !X#J 27. V2) +7*6+7)+1 641@*+012*+-7 L6-L46*+4) *V2* .46+<4 T6-M 2 .+W4647* 1V27@74= 1-7.,1*2714 2* 74B2*+<4 27. L-)+*+<4 <-=*2B4)'L64),M2R=> -Z+7B *- 27 2)>MM4*6+1 .+)*6+R,*+-7 -T0[4. 1V26B4) -7 *V4 L-64X C,R)*+*,*+-7 -T 1V=-6+.4 Z+*V.+W4647* 27+-7) 64<42=) *V4 T-==-Z+7B )4=41*+<+*> )4@a,4714 %b!

# " $=!cA!cB=,1-72*4!' ),BB4)*+7B*V2* *V4 L46M42*+-7 L-64 +) 0==4. Z+*V Z2*46X ?V4L6-L46*+4) -T *V4 CH"GD 1V2774=) +7 <21,-=26 M4M@R6274) 264 )+M+=26 *- *V-)4 -R)46<4. +7 L=2726 =+L+.M4MR6274) L64L264. Z+*V 2)-=41*+7X ?V+) Z-6d L6-@<+.4) 2 .+641* .4M-7)*62*+-7 -T *-[+7 4W41*) -7 2 72*+<4L=27* M4MR6274' 4[*47.+7B *- 2 R+-=-B+12= )>)*4ML64<+-,) 64),=*) -R*2+74. -7 26*+01+2= L=2726 =+L+.M4MR6274)X

G#% H'0-.I (-7 1V2774=) e H2*1V 1=2ML e D7+-7)4=41*+<+*>

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233+#4,)1,&("5 CH"GDQ )>6+7B-L4L*+7 "GDf C&hQ )>6+7B-M>1+7 hfUKHQ =+L-.4L)+L4L*+.4f HU5Q L=2726 =+L+. M4MR6274)f C3Q )=-Z<21,-=26 I1V2774=Jf H$Q LV-)LV2*+.>=1V-=+74f HhQ LV-)LV2*+.>=4*V@27-=2M+74f HCQ LV-)LV2*+.>=)46+74f UiHQ =+a,+. j,71*+-7 L-*47*+2=f62Q 2114)) 64)+)*2714f hK?DQ 4*V>=474.+2M+74*4*62214*+1 21+.X

iX 54MR6274 /+-=X !EE' "#_k"9E I"FF"JKb(Q !FX!FF_S)FF"#"@FF!@F!E_@[

7&++#"8&(%#(0# 1&5 DX $26L274*-' 4M2+=Q 126L274*l+1RXB4X176X+*

*V464R> R4+7B +7<-=<4. +7 2 <26+4*> -T L=27* .+)42)4)X?V4 L6-.,1*+-7 -T UKH)' +7 L26*+1,=26 CH"GD' .,6+7BL=27* +7T41*+-7 Z2) 64147*=> .4M-7)*62*4. R> 27 +M@M,7-=-B+12= 2LL6-21V IA-B=+27- 4* 2=X' !:::JX

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M4MR6274 -T L=27* 14==)' )4<462= =+74) -T 4<+.4714+7.+12*4 *V2* 2=)- +7*6214==,=26 M4MR6274) M2> R42W41*4.X ?V+) +) ),BB4)*4. R>Q !J *V4 12L21+*> -T .4@)*2R+=+N+7B 27. 16-))+7B *V4 L=2)M2 M4MR6274 I$2@M-7+ 4* 2=X' !::GJ' "J *V4 1=-),64 -T =42T )*-M2*2+7.,14. R> *V4 *-[+7 IK+ ;+-6B+- 4* 2=X' !::82J IZV+1V+7<-=<4) 2 64.+)*6+R,*+-7 -T <21,-=26 +-7) 27. 2.41642)4 -T *V4 <21,-=26 <-=,M4 I521&-RR+4' "FFFJJ'#J *V4 )*6+d+7B 4W41*) +7.,14. R> *V4 *-[+7 -7 +)-=2*4.M+*-1V-7.6+2 2* ),RM+16-M-=26 .-)4) IK+ ;+-6B+-4* 2=X' !::8RJX D1*,2==>' UKH) 264 +7 B47462= 21*+<42B2+7)* 2 <26+4*> -T M4MR6274)' *V-,BV 2 M26d4..4L47.4714 ,L-7 =+L+. 1-ML-)+*+-7 V2) R447 -R@)46<4. Ii,=M27-L 4* 2=X' !::#f $2M-7+ 4* 2=X' !::GfK2==2 C4662 4* 2=X' !:::2JX

Y464 Z4 V2<4 ,)4. *V4 L=27* <21,-=4' +X4X' *V4+7*6214==,=26 )*-62B4 -6B274==4 *V2* -11,L+4) ,L *-:F! -T *V4 1>*-L=2)M+1 <-=,M4 -T L=27* 14==)' 2) 274Z M-.4= )>)*4M T-6 )*,.>+7B *V4 M-.4 -T 21*+-727. *V4 1V2774=@T-6M+7B 12L21+*> -T UKH)X ?V4

9)2A JA C+7B=4@1V2774= *627)+*+-7) -T +-7 1V2774=) T-6M4. R> CH"GD+7 2)-=41*+7 L=2726 =+L+. R+=2>46)X H274=) 2 27. 9Q 64L64)47*2*+<4*6214)' .+)L=2>+7B )+7B=4@1V2774= *627)+*+-7) -T CH"GD@+7.,14.1,6647*' +7 )>MM4*6+12= )-=,*+-7) IC-=,*+-7 $J 2* *V4 +7.+12*4.<-=*2B4)X D) 2 64),=* -T *V4 B2*+7B M41V27+)M' +7 *V4 +7+*+2= L-6*+-7-T *V4 641-6.)' 1V2774=) -L47 2* 74B2*+<4 <-=*2B4) IL274= 2' *6214)2* !9F 27. !8F M3J 27. 1=-)4 2* L-)+*+<4 <-=*2B4) IL274= 9' *6214)2* ^8F 27. ^EF M3JX ?V4 .+W4647* -L47 =4<4=) I+7.+12*4. R> b+'ZV464 + n !' "' ! ! ! ( +) *V4 7,MR46 -T )+7B=4 1V2774=) )+M,=*2@74-,)=> -L47J 264 +.47*+04. R> .2)V4. =+74)X b7 *V4 6+BV*' *V4 -1@1,L2*+-7 V+)*-B62M) -T *V4 1-664)L-7.+7B =4<4=) 264 64L-6*4.X H274=

7Q ;@< 1V2621*46+)*+1 -T 2 )+7B=4 CH"GD 1V2774=X h21V 1,6647* 2M@L=+*,.4 +) .46+<4. T6-M *V4 1,6647* )*4L) -R)46<4. +7 4[L46+M47*)=+d4 *V-)4 64L-6*4. +7 *V4 ,LL46 L274=)X ?V4 ;@< 1,6<4 +) 7-7=+7426'+X4X' 1-7.,1*2714 2* 74B2*+<4 2LL=+4. <-=*2B4) I-!J +) =26B46 *V27*V2* 2* L-)+*+<4 <-=*2B4) I-^JX ?V4 *Z- =+M+*+7B )=-L4 1-7.,1*2714)264 I%)"=#% :,(#"J -! n 9G ` !!' LC' -^ n !GX8 ` FX# LC' L6-@<+.+7B -!SB^ n "X: ` FX_X A+72= CH"GD 1-7147*62*+-7 Z2) !"XG75X D *-*2= -T "FF )+7B=4@1V2774= *627)+*+-7)' *2d47 T6-M " .+W4647*4[L46+M47*)' Z464 272=>N4.X H274= .Q H6+M26> )*6,1*,64 -T CH"GDX%-7@)*27.26. 2M+7- 21+.) 264Q K2R' "'9@.+2M+7-R,*27-+1 21+. 27.KVR' "'#@.4V>.6-@"@2M+7-R,*>6+1 21+.f &Q #@V>.6-[>.4127->=X

"#E DX $26L274*- 4* 2=XQ C>6+7B-L4L*+7 "GD A-6M) (-7 $V2774=) +7 ?-7-L=2)*)

L46M42R+=+N+7B 21*+<+*> -T CH"GD -7 <21,-=26 M4M@R6274) I*-7-L=2)*)J Z2) )*,.+4. Z+*V *V4 L2*1V@1=2ML*41V7+a,4X $-ML264. *- 26*+01+2= M4MR6274) 1-M@L-)4. -T L,64 =+L+.)' *V4 <21,-=4 +) 2 T,==> 72*,62=M4MR6274 *V2* 1-7*2+7) 2 <26+4*> -T =+L+.) ILV-)@LV-=+L+.)' B=>1-=+L+.) 27. 74,*62= =+L+.) I?2<467+46'U4 o,-1 g U4 o,-1' !::#f /4VN2.+L-,6 4* 2=X' !::EJJ

2) Z4== 2) L6-*4+7) *V2* M2> 21* 2) 64B,=2*-6)' -6 4<476414L*-6)' T-6 CH"GDX ?V464T-64' CH"GD 21*+-7 -7 *V+)R+-=-B+12==> 1-ML=4*4 M4MR6274 M2> .+W46 )+B7+0@127*=> 4<47 T6-M *V2* -7 *V4 )>7*V4*+1 1-,7*46L26*)X(7 2..+*+-7' *V4 *-7-L=2)* V2) 1-7)+.462R=4 *41V7+12=2.<27*2B4) Z+*V 64)L41* *- -*V46 72*,62= M4MR6274)'),1V 2) *V4 42)> +)-=2*+-7' *V4 L-))+R+=+*> -T M2d+7BT2)* 27. .,62R=4 )42=)' 27. *V2* -T L6-<+.+7B 64=+2R=41-7*6-= 1-7.+*+-7) M42),6+7B 47.-B47-,) <21,-=261V2774=) I;2MR2=4 4* 2=X' !::8f $26L274*-' $27*,P g;2MR2=4' !:::f "FF!JX

C<&#0)<=. <1- C#&"'-.

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CH"GD Z2) L64L264. 27. L,6+04. 2) L64<+-,)=> .4)16+R4. I/2==+-4* 2=X' !::!JX (*) 1-7147*62*+-7 +7 )*-1d )-=,*+-7) Z2) .4*46M+74. R>2M+7-@21+. 272=>)+) 27. a,27*+012*+-7 R> U$@5C 2) .4)16+R4.I5-7*+ 4* 2=X' "FF!JX ?V4 =+L+. ,)4. +7 HU5 4[L46+M47*) Z2) )->@R427 2)-=41*+7 64L,6+04. 211-6.+7B *- ]2B2Z2 27. &21d46 I!:_!JT6-M 2 1-MM461+2= L6-.,1* IC+BM2' C*X U-,+)' 5bJX D11-6.+7B *-L64<+-,) 272=>)+) IK4M4= 4* 2=X' !::!J' +* V2. *V4 T-==-Z+7B 1-M@L-)+*+-7Q LV-)LV2*+.>=1V-=+74' "9!f LV-)LV2*+.>=4*V27-=2M+74'#:!f LV-)LV2*+.>=)46+74' !:!f LV-)LV2*+.+1 21+.' 8! LV-)LV2*@+.>=+7-)+*-= !!f =>)- .46+<2*+<4) :!f -*V46 LV-)LV-=+L+.) "!X &4@2B47*) Z464 2== *V4 R4)* B62.4 2<2+=2R=4 27. Z464 ,)4. Z+*V-,*T,6*V46 L,6+012*+-7X

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^s<21 264 *V4 )>MM4*6+12= L-*2))+,M 21*+<+*+4) +7 *V41>*-)-= 27. +7 *V4 <21,-=4f !D' !$=' !] 264 *V4 27+-7' 1V=-6+.4 27.L-*2))+,M L46M42R+=+*+4)' 64)L41*+<4=>X <64< +) *V4 64<46)2= <-=*2B4M42),64. +7 *V4 L64)4714 -T 421V 27+-7X D1*+<+*> 1-4t1+47*) Z464*2d47 T6-M &-R+7)-7 27. C*-d4) I!:G:J 27. H+*N46 I!:_:JX \4 ,)4.FX_9!' FX_"8' FX_99 27. FX_G8' 64)L41*+<4=>' T-6 ]A' ]%b#' ]$= 27.%2$=X ?V4 21*+<+*> 1-4t1+47* -T ]B=,1-72*4 Z2) 2)),M4. *- R41-ML262R=4 *- *V2* -T -*V46 L-*2))+,M )2=*) -T -6B27+1 27+-7)R426+7B 2 126R-[>= B6-,L I4XBX' ]YM2=-72*4 27. ]Y),11+72*4J 27.*V464T-64 4)*+M2*4. *- R4 FX_"X ?V4 M4MR6274 12L21+*> 27. *V42114)) 64)+)*2714 I62J -T *V4 <21,-=4 Z464 M42),64. ,)+7B *V41-ML47)2*+-7 1+61,+*6> -T *V4 L2*1V@1=2ML 2ML=+046 IU+)* hH$_JX(7 ZV-=4@<21,-=4 M42),64M47*)' *V4 2LL=+4. <-=*2B4 Z2) 1-6641*4.

9)2A KA $,6647*@<-=*2B4 1V2621*46+)*+1) -T *V4 CH"GD 1V2774=X I2JDT*46 *V4 2LL=+12*+-7 -T ! !5 CH"GD +7 *V4 )*27.26. R2*V )-=,*+-7IT-6 "F )41J' M216-)1-L+1 1,6647*) Z464 4=+1+*4. R> 2 )46+4) -T <-=*2B4L,=)4) 627B+7B T6-M !_F M3 *- ^_F M3 +7 !F@M3 )*4L)X Y-=.+7B27. *2+= L-*47*+2=) Z464 2* F 27. !GF M3' 64)L41*+<4=>X $>*-L=2)@M+1@)+.4@-,* 4[1+)4.@L2*1V Z2) ,)4.X @88#+ 1+)0#"Q CH"GD@M4.+2*4.

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