Lignin Biosynthesis in Stem Rust Infected Wheat - ACS Symposium

Chapter 27

Lignin Biosynthesis in Stem Rust Infected Wheat

Downloaded by UNIV OF MICHIGAN ANN ARBOR on February 18, 2015 | http://pubs.acs.org Publication Date: July 31, 1989 | doi: 10.1021/bk-1989-0399.ch027

Bruno M . Moerschbacher Institut für Biologie III (Pflanzenphysiologie) der RWTH Aachen, Worringerweg, D-5100 Aachen, Federal Republic of Germany

Highly resistant wheat varieties exhibit a typical hypersensitive response when infected with an avirulent race of the stem rust fungus. Host cells which are penetrated by a fungal haustorium undergo rapid necrotization, thus depriving the biotrophic parasite of its nutritional basis. This rapid cell death is correlated with the deposition of lignin or lignin-like material in the host cell walls and protoplasts. Inhibition of lignin biosynthesis delays necrotization of penetrated host cells and partially breaks resistance of wheat to stem rust. In resistant plants, an increase in the activities of the general phenylpropanoid pathway and of the specific branch pathway of lignin biosynthesis can be detected at the time of the hypersensitive cell death, contrasting to decreased activities in susceptible near-isogenic plants. The participation of both an elicitor and a suppressor in the signal exchange between host and parasite has been suggested. An elicitor of lignification could be isolated from fungal cell walls. An endogenous suppressor of the resistance reaction was found in wheat cell walls. L i g n i n , the second most a b u n d a n t organic c o m p o u n d o n e a r t h , is e x t r e m e l y resistant t o m i c r o b i a l d e g r a d a t i o n (1,2) a n d thus constitutes one o f t h e most effective m e c h a n i c a l barriers against pathogenic i n v a s i o n (3,4). C o n sequently, t h e l i g n i n content o f higher plants has l o n g been recognized as a n i m p o r t a n t factor i n t h e resistance against t h e a t t a c k b y a m y r i a d o f p o t e n t i a l pathogens. In a d d i t i o n t o i t s role as a preformed resistance factor, Hijwegen (5) has also proposed active i n d u c t i o n o f l i g n i f i c a t i o n as a defense m e c h a n i s m of c u c u m b e r against Cladosporium. Subsequently, i n a n u m b e r o f hostp a t h o g e n i n t e r a c t i o n s , i n d u c e d l i g n i f i c a t i o n has been proposed as the a c t i v e 0097-6156/89/0399-0370$06.00/0 © 1989 American Chemical Society

In Plant Cell Wall Polymers; Lewis, N., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1989.


27.

MOERSCHRACHER

371

Stem Rust Infected Wheat

m e c h a n i s m for resistance. S o m e of the most intensely s t u d i e d i n t e r a c t i o n s are those of resistance of t o b a c c o against t o b a c c o mosaic v i r u s (6-9), p o t a t o against Phytophihora (10-12) or non-pathogens (13), c u c u m b e r (14,15) a n d melons (16-18) against Cladosporium a n d Colletotrichum species. In the f a m i l y of the G r a m i n e a e , w h i c h includes some of m a n ' s most i m p o r t a n t crops, active l i g n i f i c a t i o n seems t o be of s p e c i a l i m p o r t a n c e for i n d u c e d resistance m e c h a n i s m s (19,20). T h i s m a y be correlated w i t h the n e a r l y complete absence of p h y t o a l e x i n s i n t h i s f a m i l y (21). I n spite of a n intensive search for such i n f e c t i o n - i n d u c e d f u n g i toxic substances, n o p h y t o a l e x i n s have been f o u n d i n wheat to date (22). Nevertheless, i n d u c e d l i g n i f i c a t i o n has been s h o w n t o p l a y a n i m p o r t a n t role i n disease resistance of wheat against a v a r i e t y of f u n g a l pathogens (4): T h e f o r m a t i o n of a r i n g of lignified cells at w o u n d m a r g i n s prevents the s p r e a d of n e c r o t r o p h i c f u n g i (23-25). L i g n i f i e d p a p i l l a e p r o d u c e d i n e p i d e r m a l cells j u s t below f u n g a l appressoria prevent the ingression of f u n gal p e n e t r a t i o n pegs d i r e c t l y p e n e t r a t i n g e p i d e r m a l cells (26-29). C e l l u l a r l i g n i f i c a t i o n of p e n e t r a t e d e p i d e r m a l a n d m e s o p h y l l cells a n d c o n c o m i t a n t cell d e a t h arrest further g r o w t h of b i o t r o p h i c parasites (22,30,31). M o d e s o f A c t i o n o f L i g n i f i c a t i o n as a R e s i s t a n c e

Mechanism

Several modes of a c t i o n of l i g n i f i c a t i o n as a resistance m e c h a n i s m have been proposed b y R i d e (32). L i g n i f i c a t i o n enhances the resistance of p l a n t cell walls against m e c h a n i c a l a n d e n z y m a t i c a t t a c k a n d m a y t h u s i m p e d e f u n g a l i n v a s i o n of host cells. I n c r u s t a t i o n of cell w a l l s w i t h l i g n i n m a y slow d o w n diffusion a n d t h u s i m m o b i l i z e f u n g a l toxins or decrease the flow of n u t r i e n t s t o the parasite. T h e phenolic precursors as w e l l as the free r a d i c a l s f o r m e d d u r i n g the process of l i g n i f i c a t i o n m a y be f u n g i t o x i c a n d act as p h y t o a l e x i n s . F u r t h e r m o r e , l i g n i f i c a t i o n m a y spread t o h y p h a l walls and thus impede further fungal growth. O n e or several of these m e c h a n i s m s m a y be i n v o l v e d i n resistance responses w h e n l i g n i f i c a t i o n takes place i n the p l a n t cell w a l l s . I n the case of b i o t r o p h i c parasites w h i c h rely o n f u n c t i o n a l m a t u r e h a u s t o r i a w i t h i n l i v i n g host cells for their development (33-36), l i g n i f i c a t i o n of the w h o l e cell contents l e a d i n g t o r a p i d host cell d e a t h m a y i n itself be a decisive factor i n the expression of resistance. E v i d e n c e for t h e P a r t i c i p a t i o n o f L i g n i f i c a t i o n i n R e s i s t a n c e actions

Re-

Different approaches have been used to p r o d u c e evidence for the p a r t i c i p a t i o n of l i g n i f i c a t i o n i n resistance reactions. W e w i l l confine the discussion t o those techniques a p p l i e d i n investigations o n resistance reactions of w h e a t , one of the best s t u d i e d host p l a n t s to date (4). T h e most convenient way of d e t e r m i n i n g l i g n i n is p r o v i d e d b y a range of h i s t o c h e m i c a l s t a i n i n g reactions (37): A p o s i t i v e o u t c o m e of the p h l o r o g l u c i n o l / H C l or the c h l o r i n e / s u l f i t e test, supposed to be the most specific s t a i n s for l i g n i n (38,39), p o i n t t o the p a r t i c i p a t i o n of l i g n i n i n the i n v e s t i g a t e d resistance p h e n o m e n a (23-25,28-31).



372

PLANT C E L L W A L L P O L Y M E R S

Y e l l o w autofluorescence of l i g n i n i n U V - l i g h t (40,41) has also been used as a c r i t e r i o n (28,30,31). However, i n v i e w of the countless autofluorescent substances i n p l a n t s (40,42), even the r e c o r d i n g of a t y p i c a l e m i s s i o n spect r u m for l i g n i n (31) cannot be regarded as a specific p r o o f for the presence of l i g n i n . T h e decreased e n z y m a t i c d i g e s t i b i l i t y of p l a n t cell w a l l s u p o n i n c r u s t a t i o n w i t h l i g n i n (1,2,32) has also been used as a n , albeit quite unspecific, d e m o n s t r a t i o n of l i g n i f i c a t i o n (23,24,28-30). T h e b i o c h e m i c a l d e t e r m i n a t i o n of n e w l y synthesized l i g n i n is difficult because of large a m o u n t s of preformed l i g n i n i n t r a c h e a r y a n d s u p p o r t i n g elements of h e a l t h y tissues. Nevertheless, i t has been achieved i n the case of non-host resistance reactions against w o u n d infections b y n e c r o t r o p h i c parasites (23). W h e n r a d i o a c t i v e l i g n i n precursors are a p p l i e d t o resistant host p l a n t s infected w i t h a n a v i r u l e n t p a t h o g e n , the a u t o r a d i o g r a p h i c l o c a l i z a t i o n of r a d i o a c t i v i t y i n resistant r e a c t i n g host cells m a y help to c o r r o b o r a t e the p a r t i c i p a t i o n of l i g n i f i c a t i o n i n the resistance response. T h o r o u g h e x t r a c t i o n of n o n - p o l y m e r i z e d precursor w i t h organic solvents a n d the r e m o v a l of esterified phenolics b y alkaline h y d r o l y s i s are i m p o r t a n t steps i n these e x p e r i m e n t s (25,28,30,31). A different a p p r o a c h to investigate active l i g n i f i c a t i o n d u r i n g resistance reactions is p r o v i d e d b y the d e t e r m i n a t i o n of e n z y m e a c t i v i t i e s i n v o l v e d i n l i g n i n biosynthesis. R e s i s t a n t plants are expected t o be more s t r o n g l y a c t i v a t e d d u r i n g or i m m e d i a t e l y preceding the resistance r e a c t i o n c o m p a r e d to susceptible p l a n t s . T h u s , p h e n y l a l a n i n e a m m o n i a - l y a s e ( P A L ) (43-45), c i n n a m i c a c i d 4-hydroxylase (46), O-methyltransferases (44), a n d 4 - c o u m a r a t e : C o A ligase (46) have been investigated i n a n u m b e r of s t u d ies. A s these enzymes are p a r t of the general p h e n y l p r o p a n o i d p a t h w a y , a n d t h u s not j u s t i n v o l v e d i n l i g n i n biosynthesis, t h e i r a c t i v a t i o n is o n l y p r o o f of o v e r a l l p a r t i c i p a t i o n of phenolic substances i n the resistance reactions (47-49). I n order to prove a specific i n d u c t i o n of l i g n i f i c a t i o n , one or several enzymes of the specific b r a n c h p a t h w a y of l i g n i n biosynthesis must be i n v e s t i g a t e d . A l t h o u g h peroxidases catalyze the last e n z y m i c step of t h i s p a t h w a y (50), increased peroxidase a c t i v i t i e s cannot be regarded as a specific c r i t e r i o n for l i g n i f i c a t i o n , as these enzymes p l a y a range of different roles i n p l a n t m e t a b o l i s m (51). Lignification i n the W h e a t - S t e m

Rust

System

W e w i l l n o w consider the evidence t h a t has a c c u m u l a t e d to show the p a r t i c i p a t i o n of l i g n i f i c a t i o n i n the hypersensitive resistance of wheat t o the wheat s t e m rust fungus, Puccinia graminis f. sp. tritici. B e a r d m o r e et al (30) a n d T i b u r z y (31) showed t h a t e p i d e r m a l (31) a n d m e s o p h y l l (30,31) cells of resistant wheat p l a n t s , p e n e t r a t e d b y h a u s t o r i a of a n a v i r u l e n t race of the fungus, can be s t a i n e d w i t h p h l o r o g l u c i n o l / H C l (31) a n d c h l o r i n e / s u l f i t e (30,31). These cells show yellow a u t o f l u o rescence u n d e r U V - l i g h t (30,31), the emission s p e c t r u m is i d e n t i c a l t o t h a t of l i g n i f i e d t r a c h e a r y elements (31).



27.

MOERSCHBACHER


373

T h e a p p l i c a t i o n of r a d i o a c t i v e p h e n o l i c p r e c u r s o r s — q u i n i c a c i d a n d s h i k i m i c a c i d (52), p h e n y l a l a n i n e (30,53), t y r o s i n e (53), a n d c i n n a m i c a c i d ( 3 0 , 3 1 , 5 3 ) — t o infected wheat leaves led to a solvent- a n d a l k a l i - r e s i s t a n t i n c o r p o r a t i o n o f r a d i o a c t i v i t y i n t o h y p e r s e n s i t i v e l y r e a c t i n g host cells s u g gesting lignin formation h a d occurred. I n a recent s t u d y (54), we showed increased a c t i v i t i e s o f t w o enzymes o f the general p h e n y l p r o p a n o i d p a t h w a y , P A L a n d 4 - c o u m a r a t e : C o A l i g ase, as w e l l as one e n z y m e of the specific p a t h w a y o f l i g n i n b i o s y n t h e s i s , c i n n a m y l - a l c o h o l dehydrogenase ( C A D ) , i n resistant p l a n t s at the t i m e of the h y p e r s e n s i t i v e host cell d e a t h . O n the other h a n d , decreased a c t i v i t i e s were observed at the same t i m e w i t h susceptible host p l a n t s (54). Furt h e r m o r e , we showed t h a t the w e l l k n o w n increase i n peroxidase a c t i v i t i e s , w h i c h is s t r o n g i n resistant a n d o n l y weak i n susceptible p l a n t s (55-58), is at least p a r t l y due to the increased a c t i v i t y of the l i g n i n b i o s y n t h e t i c p a t h w a y (54,59). W h e n h i g h l y resistant wheat varieties are i n o c u l a t e d w i t h a n a v i r u l e n t race of the s t e m rust fungus, f u n g a l g r o w t h is arrested b y the h y p e r s e n s i tive d e a t h o f the first p e n e t r a t e d host cells (30,31.) E v e n i n v e r y densely i n o c u l a t e d leaves, the r e a c t i o n of less t h a n one percent of the host cells is sufficient to s t o p f u r t h e r development o f the p a r a s i t e . T h i s s m a l l percentage m a y be the reason, w h y no increased content o f b i o c h e m i c a l l y d e t e r m i n e d l i g n i n was measured i n infected hypersensitive wheat leaves (60,61). H o w e v e r , w h e n a n e l i c i t o r (see b e l o w ) , i s o l a t e d f r o m the s t e m rust fungus (62), is injected i n t o the i n t e r c e l l u l a r spaces o f wheat leaves almost every cell i n the i n f i l t r a t e d area e x h i b i t s a h y p e r s e n s i t i v e - l i k e r e a c t i o n (6265). I n the e l i c i t o r treated leaves, l i g n i n content as d e t e r m i n e d b y the t h i o g l y c o l i c a c i d procedure clearly increased (66). L i g n i f i c a t i o n as a C a u s a l F a c t o r i n

Resistance

T h e above described studies s t r o n g l y suggest a c o r r e l a t i o n between l i g n i fication a n d resistance. H o w e v e r , they do not allow any c o n c l u s i o n c o n c e r n i n g a c a u s a l r e l a t i o n s h i p between the two p h e n o m e n a . T h e q u e s t i o n r e m a i n s as t o w h e t h e r l i g n i f i c a t i o n is indeed responsible for i m p a i r e d f u n g a l development. W e have a l r e a d y briefly m e n t i o n e d a possible c h a i n o f events d u r i n g the i n c o m p a t i b l e i n t e r a c t i o n between h i g h l y resistant wheat leaves a n d a v i r u l e n t s t r a i n s of the s t e m rust fungus. L i g n i f i c a t i o n of the w h o l e cell contents m a y be regarded as a n active m e c h a n i s m for the p e n e t r a t e d host cell to c o m m i t " s u i c i d e " (30,31). T h i s h y p e r s e n s i t i v e cell d e a t h i n t u r n is t h o u g h t t o be responsible for the arrest of f u n g a l g r o w t h , p o s s i b l y b y d e p r i v i n g the obligate parasite o f its n u t r i t i o n a l basis (67,68.) T h e first step t h u s postulates l i g n i f i c a t i o n as the m e c h a n i s m o f a c t i v e cell d e a t h . C e l l d e a t h , a genetically p r o g r a m m e d event associated w i t h a c t i v e processes (69,70), is closely correlated w i t h l i g n i f i c a t i o n i n a range of different d e v e l o p m e n t a l p r o g r a m s : firstly, senescence is often a c c o m p a n i e d b y increased l i g n i f i c a t i o n (71,72); secondly, l i g n i f i c a t i o n is one o f the m o s t p r o m i n e n t reactions d u r i n g w o u n d h e a l i n g (73-79); a n d t h i r d l y , l i g n i f i c a t i o n o f d y i n g cells i n v a r i a b l y o c c u r s d u r i n g x y l e m d i f f e r e n t i a t i o n (80). A direct



374

PLANT C E L L W A L L POLYMERS

cause-effect r e l a t i o n s h i p of l i g n i f i c a t i o n a n d cell d e a t h has been described recently (81). T h e second step of the proposed c h a i n of events, resistance as a direct consequence of cell d e a t h , is s t i l l controversial (82-86). I n the w h e a t - s t e m rust s y s t e m , evidence f a v o u r i n g the i d e a of hypersensitive cell d e a t h as the cause of resistance (30,31,87-90) contrasts to results suggesting cell collapse as b e i n g a mere consequence of a yet u n k n o w n p r e c e d i n g resistance m e c h a n i s m (90-97). R e c e n t l y , K o g e l et al. (98) showed t h a t the i n j e c t i o n of galactoseb i n d i n g lectins or the e n z y m e galactose oxidase i n t o resistant wheat leaves p r e v e n t e d the hypersensitive cell d e a t h of p e n e t r a t e d host cells a n d c o n c o m i t a n t l y led t o increased f u n g a l g r o w t h , suggesting a causal r e l a t i o n s h i p between hypersensitive cell d e a t h a n d resistance. T i b u r z y (22,31) o b t a i n e d s i m i l a r results b y a p p l i c a t i o n of the P A L i n h i b i t o r a m i n o o x y a c e t i c a c i d ( A O A ) . However, A O A does not specifically i n h i b i t P A L (99), a n d P A L is not o n l y i n v o l v e d i n l i g n i n biosynthesis (100). T h u s , A O A a n d the related i n h i b i t o r a m i n o o x y p h e n y l p r o p i o n i c a c i d ( A O P P ) (101,102) i n h i b i t the biosynthesis of l i g n i n (103,104), a n t h o c y a n i n s (105), other flavonoids (106), a n d conjugates of c i n n a m i c acids (107) v i a P A L , as well as ethylene (108-110) v i a a p y r i d o x a l p h o s p h a t e dependent e n z y m e (110,111). I n v i e w of the possible f u n c t i o n of phenolic c o m p o u n d s as p h y t o a l e x i n s (21,112,113) a n d the w e l l d o c u m e n t e d role of ethylene i n some resistance reactions (114-116), the above c i t e d e x p e r i m e n t s w i t h A O A (22, 31) do not p r o v i d e any conclusive evidence for a causal role of l i g n i f i c a t i o n i n resistance. O u r recent observation (Moerschbacher & N o l l , u n p u b l i s h e d ) t h a t a different P A L i n h i b i t o r , ( l - a m i n o - 2 - p h e n y l e t h y l ) p h o s p h o n i c a c i d ( A P E P ) , is e q u a l l y a c t i v e i n p r e v e n t i n g hypersensitive cell d e a t h a n d p a r t i a l l y l o w e r i n g resistance of wheat to s t e m rust s t r o n g l y suggest t h a t the effects of b o t h i n h i b i t o r s is v i a their i n h i b i t o r y a c t i o n against P A L . Besides these w e l l k n o w n P A L i n h i b i t o r s , h i g h l y specific suicide i n h i b i t o r s of C A D are n o w available (117,118). These i n h i b i t o r s combine two i m p o r t a n t features: they act as s u b s t r a t e analogues a n d are able t o specifi c a l l y c o m p l e x z i n c ions. T h e c o m b i n a t i o n of these properties guarantees the h i g h specificity of these substances. Besides C A D , o n l y c i n n a m o y l : C o A reductase is i n h i b i t e d , b o t h enzymes are o n l y i n v o l v e d i n l i g n i n biosynthesis (119). T h e m e c h a n i s m of i n h i b i t i o n is t h o u g h t to be a pseudo-irreversible i n a c t i v a t i o n of the suicide type (120). S u c h i n h i b i t o r s are i d e a l l y s u i t e d for in-vivo assays, as they are h i g h l y specific a n d generally s l o w l y m e t a b o l i z e d (121). T h e a p p l i c a t i o n o f two o f these i n h i b i t o r s , N ( O - h y d r o x y p h e n y l ) s u l f i n a m o y l - t e r t i o b u t y l acetate a n d N ( O - a m i n o p h e n y l ) s u l f i n a m o y l - t e r t i o b u t y l acetate, to h i g h l y resistant wheat leaves infected w i t h a n a v i r u l e n t s t r a i n of s t e m rust r e s u l t e d i n decreased l i g n i f i c a t i o n a n d decreased necrosis of p e n e t r a t e d host cells a n d c o n c o m i t a n t l y led to increased f u n g a l development, o c c a s i o n a l l y even a l l o w i n g some s p o r u l a t i o n t o occur (60). T h e described i n h i b i t i o n of hypersensitive cell d e a t h b y the C A D i n -


27.

MOERSCHBACHER


375


h i b i t o r s s t r o n g l y suggests a causal r e l a t i o n s h i p between l i g n i f i c a t i o n a n d cell d e a t h . It c a n f u r t h e r be c o n c l u d e d f r o m the increase o f f u n g a l g r o w t h u p o n C A D i n h i b i t i o n t h a t the synthesis of the m o n o m e r i c l i g n i n p r e c u r sors is c a u s a l l y related to resistance of wheat to s t e m r u s t . H o w e v e r , i t r e m a i n s s p e c u l a t i v e whether the p o l y m e r i z a t i o n of these m o n o m e r s to the t h r e e - d i m e n s i o n a l network of l i g n i n itself is a prerequisite for resistance. F u r t h e r m o r e , the proposed causal r e l a t i o n s h i p between cell d e a t h a n d resistance cannot be c o n c l u d e d f r o m these e x p e r i m e n t s ; b o t h p h e n o m e n a m a y be i n d e p e n d e n t results of the l i g n i f i c a t i o n process. Elicitation of Lignification T h e t e r m e l i c i t o r , i n i t i a l l y defined as a f u n g a l m e t a b o l i t e c a p a b l e o f i n d u c i n g p h y t o a l e x i n p r o d u c t i o n w h e n a p p l i e d to host p l a n t s (122, 123), has since been a p p l i e d to p a r a s i t e - d e r i v e d molecules w h i c h i n d u c e a n y facet o f resistance i n a p p r o p r i a t e host p l a n t s , i n c l u d i n g l i g n i f i c a t i o n (124). T h e work of R i d e a n d his coworkers (24,125,126) showed t h a t p r o d u c t s o f filamentous f u n g i are able to e l i c i t l i g n i f i c a t i o n at w o u n d m a r g i n s i n wheat leaves. C h i t i n a n d some of its soluble derivatives have been s h o w n to be e l i c i t o r s o f l i g n i f i c a t i o n i n wheat (125), c h i t o s a n b e i n g m o r e a c t i v e t h a n c h i t i n (62,126). M o s t other /?-glucans i n c l u d i n g l a m i n a r i n d i d n o t e x h i b i t e l i c i t o r a c t i v i t y (62, 126). A crude e x t r a c t of Phytophthora megasperma f. sp. glycinea cell w a l l s , capable of i n d u c i n g g l y c e o l l i n a c c u m u l a t i o n i n soybeans, also e l i c i t e d l i g n i f i c a t i o n i n wheat (126), b u t p u r i f i e d e l i c i t o r f r o m the same source (62) a n d the s y n t h e t i c hepta-/?-glucoside e l i c i t o r (126) were ineffective. W e have p r e v i o u s l y r e p o r t e d the p u r i f i c a t i o n o f a n e l i c i t o r active f r a c t i o n f r o m cell walls of g e r m i n a t e d s t e m rust uredospores w h i c h induces l i g n i f i c a t i o n w h e n injected i n t o the i n t e r c e l l u l a r spaces of w h e a t leaves (62,63). Besides l i g n i f i c a t i o n , t h i s e l i c i t o r induces other s y m p t o m s t y p i c a l o f the h y persensitive r e a c t i o n , s u c h as m e m b r a n e d e g r a d a t i o n detected as increased a c t i v i t i e s of lipoxygenase (64) a n d phospholipase (65). T h e h i g h m o l e c u l a r weight w a t e r - s o l u b l e e l i c i t o r has been characterized as a heat s t a b l e g l y c o p r o t e i n w i t h the c a r b o h y d r a t e m o i e t y b e a r i n g the active p a r t ( s ) of the molecule(s) (62). Recent work identified a g l y c o p r o t e i n w i t h a b o u t e q u a l a m o u n t s o f galactose a n d mannose a n d almost no glucose as the m o s t a c t i v e c o m p o n e n t (127). I n i t i a l l y , a gene specific effect of t h i s e l i c i t o r c o n c e r n i n g the 5r«5-gene for resistance o f wheat to s t e m rust was r e p o r t e d (63). However, t h i s was not c o n f i r m e d i n later w o r k (66): E l i c i t o r s p r e p a r e d f r o m t w o races o f the s t e m rust fungus differing i n t h e i r s p e c t r u m o f genes for a v i r u l e n c e were e q u a l l y a c t i v e , a n d near-isogenic wheat lines c o n t a i n i n g different genes for resistance reacted s i m i l a r to b o t h e l i c i t o r s . T h e observed differences i n r e a c t i v i t y to e l i c i t o r s between different wheat c u l t i v a r s t u r n e d o u t to be u n r e l a t e d to a n y k n o w n resistance genes. S i m i l a r results h a d been r e p o r t e d p r e v i o u s l y for a n e l i c i t o r i s o l a t e d f r o m i n t e r c e l l u l a r w a s h i n g fluids of leaf rust infected wheat leaves w h i c h i n d u c e d b r o w n i n g a n d chlorosis (128,129). T h e r e a c t i v i t y of wheat c u l t i v a r s


376


t o t h i s e l i c i t o r was dependent o n a gene o n chromosome 5 A w h i c h c o n t a i n s no k n o w n genes for seedling resistance to leaf or s t e m rust (129). It was s h o w n t h a t the same holds true for the s t e m rust e l i c i t o r (60, S u t h e r l a n d & Moerschbacher, unpublished).


W h e n injected i n t o p r i m a r y leaves of different cereals, the s t e m rust e l i c i t o r causes s y m p t o m s w h i c h closely resemble the respective resistance reactions of these species against the a t t a c k b y s t e m rust of w h e a t , i.e., l i g n i f i c a t i o n i n b a r l e y a n d rye, b r o w n spots i n oat, a n d no v i s i b l e s y m p t o m s i n m a i z e (66). T h e b i o c h e m i c a l s i m i l a r i t i e s of leaf a n d s t e m rust e l i c i t o r s , the m i s s i n g gene specificity of b o t h e l i c i t o r s , the fact t h a t a n e q u a l l y active e l i c i t o r was i s o l a t e d f r o m g e r m tube cell walls of oat c r o w n rust (60), together w i t h the described reactions of different non-hosts t o the s t e m rust e l i c i t o r led us to speculate t h a t the isolated elicitors m a y p l a y a role i n the i n d u c t i o n of general m e c h a n i s m s of non-host resistance (130). A l t h o u g h they m a y be i n v o l v e d i n the e l i c i t a t i o n of r a c e - c u l t i v a r specific resistance as w e l l , r a c e - c u l t i v a r specificity i n the w h e a t - s t e m rust s y s t e m c l e a r l y cannot b e e x p l a i n e d o n the basis of the specificity of the isolated e l i c i t o r s . O n e possible e x p l a n a t i o n w o u l d be the occurrence of r a c e - c u l t i v a r specific suppressors o f the resistance r e a c t i o n (124,131,132). P o l y g a l a c t u r o n i c a c i d has been s h o w n t o be a p o t e n t suppressor of the e l i c i t o r i n d u c e d l i g n i f i c a t i o n response i n wheat leaves (60). M o r e o v e r , p e c t i c fragments were o b t a i n e d f r o m isolated wheat cell walls b y p e c t o l y t i c digest i o n (36,60) or H F - s o l v o l y s i s ( M o e r s c h b a c h e r , R y a n , K o m a l a v i l a s , M o r t , u n p u b l i s h e d ) w h i c h suppressed the a c t i v a t i o n of l i g n i n biosynthesis w h e n injected s i m u l t a n e o u s l y w i t h e l i c i t o r . A c t i v e c o m p o n e n t s were t e n t a t i v e l y classified as fragments of h o m o g a l a c t u r o n a n a n d r h a m n o g a l a c t u r o n a n I. A n i n d e p t h c h e m i c a l c h a r a c t e r i z a t i o n as w e l l as a n e v a l u a t i o n o f possible r a c e - c u l t i v a r specificity of these "endogenous suppressors" or t h e i r in vivo p r o d u c t i o n d u r i n g c o m p a t i b l e a n d i n c o m p a t i b l e w h e a t - s t e m rust i n t e r a c t i o n s is under way. T h e i n j e c t i o n of s m a l l a m o u n t s of p e c t o l y t i c enzymes c o n c o m i t a n t l y w i t h elicitors suppressed the i n d u c t i o n of l i g n i n b i o s y n t h e t i c e n z y m e act i v i t i e s as w e l l (60). T h e i n v e s t i g a t i o n of pectic enzymes of the s t e m rust fungus (133) a n d the e l u c i d a t i o n of their substrate specificities, c o m b i n e d w i t h a d e t a i l e d a n a l y s i s of their n a t u r a l substrates, the pectic c o m p o n e n t s of p r i m a r y wheat cell w a l l s , are targets for future research. T h e h i g h l y developed r a c e - c u l t i v a r specificity i n the w h e a t - s t e m rust s y s t e m m a y be based o n the differential l i b e r a t i o n of active suppressors d u r i n g the penet r a t i o n of the host cell w a l l b y the h a u s t o r i a l neck of the fungus ( F i g u r e 1). A l t h o u g h s p e c u l a t i v e , a m o d e l can be d r a w n i n w h i c h suppressors w h i c h p o t e n t i a l l y exist i n the walls of a l l wheat varieties are set free o n l y i n c o m p a t i b l e i n t e r a c t i o n s . T h e f a i l u r e of p r o d u c i n g active suppressors d u r i n g i n c o m p a t i b l e interactions w o u l d t h e n lead t o the e l i c i t a t i o n of l i g n i f i c a t i o n as the m e c h a n i s m of hypersensitive cell d e a t h a n d resistance of wheat t o stem rust.



27.

MOERSCHBACHER

cell

377


wall

degrading enzymes

cell

wall

host

cell

hypersensitive successful haustorium

cell

death

formation resistance

• susceptibility

F i g u r e 1. H y p o t h e t i c a l scheme of events l e a d i n g t o r a c e - c u l t i v a r specific resistance or s u s c e p t i b i l i t y i n the rust s y s t e m . If the substrate specificity o f the f u n g a l cell w a l l d e g r a d i n g enzymes (e.g., pectinases) is s u i t a b l e for d e g r a d a t i o n o f a specific host cell w a l l c o m p o n e n t (e.g., p a r t l y esterified p e c t i n ) , endogenous suppressors w i l l be p r o d u c e d w h i c h prevent the e l i c i t o r i n d u c e d l i g n i f i c a t i o n response, thus l e a d i n g t o s u s c e p t i b i l i t y .


378



A cknowledgment s T h e a u t h o r ' s w o r k r e p o r t e d i n t h i s c o m m u n i c a t i o n was c a r r i e d o u t u n d e r the constant advice a n d encouragement f r o m P r o f . D r . H . J . Reisener, i n c o l l a b o r a t i o n w i t h U . N o l l , B . E . F l o t t , U . W i t t e , D . Kônigs, A . W u s t e f e l d , U . G o t t h a r d t , D r . F . Schrenk, D r . M . Sutherland, D r . J . R y a n , D r . P . K o m a l a v i l a s a n d P r o f . D r . A . J . M o r t . T h e P A L i n h i b i t o r A P E P was generally provided b y Prof. D r . F . J . Schwinn, C i b a Geigy A G , Basel, Switzerl a n d . P r o f . D r . L . G o r r i c h o n , Université P a u l S a b a t i e r , T o u l o u s e , F r a n c e , k i n d l y p r o v i d e d t h e C A D i n h i b i t o r s . T h e work was s u p p o r t e d i n p a r t b y g r a n t s f r o m t h e L a n d N o r d r h e i n - W e s t f a l e n , t h e Deutsche Forschungsgem e i n s c h a f t , a n d t h e Deutscher A k a d e m i s c h e r A u s t a u s c h d i e n s t .

Literature Cited

1. Evans, C. S. Process Biochem. 1987, 22, 102-105. 2. Kirk, T. K.; Farrell, G. L. Ann. Rev. Microbiol. 1987, 41, 465-505. 3. Vance, C. P.; Kirk, T. M.; Sherwood, R. T. Ann. Rev. Phytopathol. 1980, 18, 259-288. 4. Ride, J. P. In Biochemical Plant Pathology; Callow, J. Α., Ed.; John Wiley: Chichester, 1983; pp. 215-236. 5. Hijwegen, T. Neth. J. Plant Pathol. 1963, 69, 314-317. 6. Legrand, M.; Fritig, B.; Hirth, L. Phytochem. 1976, 15, 1353-1359. 7. Legrand, M.; Fritig, B.; Hirth, L. Planta 1978, 144, 101-108. 8. Massala, R.; Legrand, M.; Fritig, B. Physiol. Plant Pathol. 1980, 16, 213-226. 9. Collendavello, J.; Legrand, M.; Fritig, B. Plant Physiol. 1983, 73, 550554. 10. Friend, J.; Reynolds, S. B.; Aveyard, M. A. Physiol. Plant Pathol. 1973, 3, 495-507. 11. Friend, J.; Thornton, J. D. Phytopathol. Z. 1974, 81, 56-64. 12. Henderson, S. J.; Friend, J. Phytopathol. Z. 1979, 94, 323-334. 13. Hammerschmidt, R. Physiol. Plant Pathol. 1984, 24, 33-42. 14. Hammerschmidt, R.; Kuc, J. Physiol. Plant Pathol. 1982, 20, 61-71. 15. Hammerschmidt, R., Boonen, A. M.; Bergstrom, G. C.; Baker, Κ. K. Can. J. Bot. 1985, 63, 2393-2398. 16. Touze, Α.; Rossignol, M. In Biochemistry Related to Specificity in Host -Plant Pathogen Interactions; Solheim, B., Raa, J., Eds.; Tromso Uni versitets, 1977; pp 227-230. 17. Grand, C.; Rossignol, M. Plant Sci. Lett. 1982, 28, 103-110. 18. Love, S. L.; Rhodes, Β. B. Hort. Sci. 1982, 17, 501. 19. Sherwood, R. T.; Vance, C. P. Phytopathol. 1980, 70, 273-279. 20. Sherwood, R. T.; Vance, C. P. In Plant Infection: The Physiological and Biochemical Basis; Asada, Y., Bushnell, W. R., Ouchi, S., Vance, C. P., Eds.; Japan Scientific Societies: Tokyo, Springer: Berlin, 1982; pp 27-44. 21. Kuc, J. A. In Encyclopedia of Plant Physiology; Heitefuss, R., Williams, P. H., Eds.; Springer: Berlin, 1976; New Series Vol. 4, pp 632-652.



27.

MOERSCHBACHER


379

22. Reisener, H. J.; Tiburzy, R.; Kogel, Κ. H.; Moerschbacher, B.; Heck, B. In Biology and Molecular Biology of Plant-Pathogen Interactions; Bailey, J. Α., Ed.; Springer: Berlin, 1986; NATO ASI Series Vol. H1, pp 141-148. 23. Ride, J. P. Physiol. Plant Pathol. 1975, 5, 125-134. 24. Pearce, R. B.; Ride, J. P. Physiol. Plant Pathol. 1980, 16, 197-204. 25. Maule, A. J.; Ride, J. P. Physiol. Plant Pathol. 1982, 20, 235-241. 26. Young, P. A. Bot. Gaz. 1926, 81, 258-279. 27. Robertson, H. T. Sci. Agric. 1932, 12, 575-592. 28. Ride, J. P.; Pearce, R. B. Physiol. Plant Pathol. 1979, 15, 79-92. 29. Bird, P. M.; Ride, J. P. Physiol. Plant Pathol. 1981, 19, 289-299. 30. Beardmore, J.; Ride, J. P.; Granger, J. W. Physiol. Plant Pathol. 1983, 22, 209-220. 31. Tiburzy, R. Ph.D. Thesis, RWTH Aachen, F.R.G., 1984. 32. Ride, J. P. Physiol. Plant Pathol. 1980, 16, 187-196. 33. Mendgen, K. Phytopathol. 1981, 71, 983-989. 34. Manners, J. M.; Gay, J. L. In Biochemical Plant Pathology; Callow, J. Α., Ed.; John Wiley: Chichester, 1983, pp 163-195. 35. Niks, R. E. Physiol. Molec. Plant Pathol. 1986, 28, 309-322. 36. Schrenk, F. Ph.D. Thesis, RWTH Aachen, F.R.G., 1988. 37. Jensen, W. A. Botanical Histochemistry. Principles and Practice; W. H. Freeman: San Francisco, 1962. 38. Sarkanen, Κ. V.; Ludwig, C. H. In Lignins: Occurrence, Formation, Structure, and Reactions; Sarkanen, Κ. V., Ludwig, C. H., Eds.; John Wiley: New York, 1971; pp 1-18. 39. Sherwood, R. T.; Vance, C. P. Phytopathol. 1976, 66, 503-510. 40. Klein, G.; Linser, H. Öster. Bot. Ζ. 1930, 79, 125-163. 41. Willemse, M. T. M. In Cell Walls '81, Proc. 2nd Cell Wall Mtg.; Robin son, D. G., Quader, H., Eds.; Wissenschaftliche: Stuttgart, 1981; pp 242-250. 42. Goodwin, R. H. Ann. Rev. Plant Physiol. 1953, 4, 283-304. 43. Green, N. E.; Hadwiger, L. Α.; Graham, S. O. Phytopathol. 1975, 65, 1071-1074. 44. Maule, A. J.; Ride, J. P. Phytochem. 1976, 15, 1661-1664. 45. Thorpe, J. R.; Hall, J. L. Physiol. Plant Pathol. 1984, 25, 363-379. 46. Maule, A. J.; Ride, J. P. Phytochem. 1983, 22, 1113-1116. 47. Friend, J. In International Review of Biochemistry, Plant Biochemistry II; Northcote, D. H., Ed.; University Park: Baltimore, 1977; Vol. 13, pp 141-182. 48. Friend, J. Rec. Adv. Phytochem. 1978, 12, 557-588. 49. Legrand, M. In Biochemical Plant Pathology; Callow, J. Α., Ed.; John Wiley: Chichester, 1983; pp 367-384. 50. Harkin, J. M.; Obst, J. R. Science 1973, 180, 296-298. 51. Gaspar, T.; Penel, C.; Thorpe, T.; Greppin, H. Peroxidases 19701980. A Survey of Their Biochemical and Physiological Roles in Higher Plants; Université de Genève, Centre de Botanique: Genève, 1982; pp 103-106.



380

PLANT

CELL

WALL

POLYMERS

52. Rohringer, R.; Fuchs, Α.; Lunderstädt, J.; Samborski, D. J. Can. J. Bot. 1967, 45, 863-889. 53. Fuchs, Α.; Rohringer, R.; Samborski, D. J. Can. J. Bot. 1967, 45, 2137-2154. 54. Moerschbacher, Β. M.; Noll, U. M.; Flott, B. E.; Reisener, H. J. Physiol. Mol. Plant Pathol. 1988, 33, 33-46. 55. Macko, V.; Woodburg, W.; Stahmann, M. A. Phytopathol. 1968, 58, 1250-1254. 56. Fric, F.; Fuchs, W. H. Phytopathol. Z. 1970, 67, 161-174. 57. Daly, J. M.; Ludden, P.; Seevers, P. Physiol. Plant Pathol. 1971, 1, 397-407. 58. Seevers, P. M.; Daly, J. M.; Catedral, F. F. Plant Physiol. 1971, 48, 353-360. 59. Flott, Β. E.; Moerschbacher, Β. M.; Reisener, H.J. New Phytol. 1989, 111, 000-000. 60. Moerschbacher, Β. M. Ph.D. Thesis, RWTH Aachen, F.R.G., 1988. 61. Chigrin, V. V.; Rozum, L. V.; Zaprometov, M. N. Fiziol. Rast. 1973, 20, 942-948. 62. Moerschbacher, B.; Kogel, Κ. H.; Noll, U.; Reisener, H. J. Z. Natur forsch. 1986, 41c, 830-838. 63. Moerschbacher, B.; Heck, B.; Kogel, Κ. H.; Obst, O.; Reisener, H. J. Z. Naturforsch. 1986, 41c, 839-844. 64. Ocampo, C. Α.; Moerschbacher, B.; Grambow, H. J. Z. Naturforsch. 1986, 41c, 559-563. 65. Ocampo, C. Α.; Grambow, H. J. New Phytol. 1987, 107, 709-714. 66. Moerschbacher, Β. M.; Flott, Β. E.; Noll, U.; Reisener, H. J. Plant Physiol. Biochem. 1989, 27, 000-000. 67. Stakman, E. C. J. Agric. Res. 1915, 4, 193-200. 68. Stakman, E. C.; Levine, M. N. Univ. Minnesota Agric. Exp., 1922, Tech. Bull. 8, 3-10. 69. Leopold, A. C. Science 1961, 134, 1727-1732. 70. Davies, I.; Sigee, D. C. Cell Ageing and Cell Death; Soc. Exp. Biol. Sem. Ser. 25; Cambridge University: Cambridge, 1984. 71. Stone, J. E.; Blundell, M. J.; Tanner, K. G. Can. J. Chem. 1951, 29, 734-745. 72. Faulkner, G.; Kimmins W. C. Phytopathol. 1975, 65, 1396-1400. 73. Rhodes, J. M.; Wooltorton, L. S. C. In Biochemistry of Wounded Plant Tissues; Kahl, G., Ed.; Walter de Gruyter: Berlin, 1978; pp 243-286. 74. Fleuriet, Α.; Deloire, A. Z. Pflanzenphysiol. 1982, 107, 259-268. 75. Garrod, B.; Lewis, B. G.; Brittain, M. J.; Davies, W. P. New Phytol. 1982, 90, 99-108. 76. Zimmermann, H. J.; Kahl, G. BIUZ 1982, 12, 49-58. 77. Geballe, G. T.; Galston, A. W. Phytopathol. 1983, 73, 619-623. 78. Biggs, A. R. Can. J. Bot. 1986, 64, 2319-2321. 79. Hudler, G. W.; Banik, M. T. Can. J. Bot. 1986, 64, 2406-2410. 80. Woolhouse, H. W. Agric. Res. 1915, 4, 123-153.



27.

MOERSCHBACHER


381

81. Carceller, M.; Davey, M. D.; Fowler, M. W.; Street, H. E. Protoplasma 1971, 73, 367-385. 82. Heath, M. C. Phytopathol. 1976, 66, 935-936. 83. Ingram, D. S. Ann. Appl. Biol. 1978, 89, 291-295. 84. Bushnell, W. R. In Plant Infection, the Physiological and Biochemical Basis; Asada, Y., Bushnell, W. R., Ouchi, S., Vance, C. P., Eds.; Japan Scientific Societies: Tokyo, Springer: Berlin, 1982; pp 97-116. 85. Doke, N.; Tomiyama, K.; Furuichi, N. In Plant Infection, the Physio logical and Biochemical Basis; Asada, Y., Bushnell, W. R., Ouchi, S., Vance, C. P., Eds.; Japan Scientific Societies: Tokyo, Springer: Berlin, 1982; pp 79-96. 86. Tomiyama, K. In Plant Infection, the Physiological and Biochemical Basis; Asada, Y., Bushnell, W. R., Ouchi, S., Vance, C. P., Eds.; Japan Scientific Societies: Tokyo, Springer: Berlin, 1982; pp 329-344. 87. Skipp, R. Α.; Samborski, D. J. Can. J. Bot. 1974, 52, 1107-1115. 88. Samborski, D. J.; Kim, W. K.; Rohringer, R.; Howes, Ν. K.; Baker, R. J. Can. J. Bot. 1977, 55, 1445-1452. 89. Harder, D. E.; Rohringer, R.; Samborski, D. J.; Rimmer, S. R.; Kim, W. K.; Chong, J. Can. J. Bot. 1979, 57, 2617-2625. 90. Rohringer, R.; Kim, W. K.; Samborski, D. J. Can. J. Bot. 1979, 57, 324-331. 91. Brown, J. F.; Shipton, W. Α.; White, Ν. H. Ann. Appl. Biol. 1966, 58, 279-290. 92. Ogle, H. J.; Brown, J. F. Ann. Appl. Biol. 1971, 67, 309-319. 93. Kiraly, Z.; Barna, B.; Ersek, T. Nature 1972, 239, 456-457. 94. Barna, B.; Ersek, T.; Mashaal, S. F. Acta Phytopathol. Acad. Sci. Hung. 1974, 9, 293-300. 95. Mayama, S.; Daly, J. M.; Rehfeld, D. W.; Daly, C. R. Physiol. Plant Pathol. 1975, 7, 35-47. 96. Mayama, S.; Rehfeld, D. W.; Daly, J. M. Phytopathol. 1975, 65, 11391142. 97. Gousseau, H. D. M.; Deverall, B. J. Can. J. Bot. 1986, 64, 626-631. 98. Kogel, K. H.; Schrenk, F.; Sharon, N.; Reisener, H. J. J. Plant Physiol. 1985, 118, 343-352. 99. John, R. Α.; Charteris, Α.; Fowler, L. J. Biochem. J. 1978, 171, 771779. 100. Harborne, J. B. In Encyclopedia of Plant Physiology; Bell, Ε. Α., Charl wood, Β. V., Eds.; Springer: Berlin, 1980; New Series Vol. 8, pp 329402. 101. Amrhein, N.; Gödeke, K. H.; Kefeli, V. I. Ber. Deutsch. Bot. Ges. 1976, 89, 247-259. 102. Amrhein, N.; Gödeke, Κ. Η. Plant Sci. Lett. 1977, 8, 313-317. 103. Holländer, H.; Kiltz, Η. H.; Amrhein, Ν. Z. Naturforsch. 1979, 34c, 1162-1173. 104. Amrhein, N.; Frank, G.; Lemm, G.; Luhmann, Η. B. Eur. J. Cell Biol. 1983, 29, 139-144. 105. Amrhein, N.; Holländer, H. Planta 1979, 144, 385-389.


382

PLANT C E L L W A L L

POLYMERS


106. 107. 108. 109. 110.

Amrhein, N.; Diederich, E. Naturwiss. 1980, 67, 40-41. Amrhein, N.; Gerhardt, J. Biochim. Biophys. Acta 1979, 583, 434-442. Amrhein, N.; Wenker, D. Plant Cell Physiol. 1979, 20, 1635-1642. Yu, Y. B.; Adams, D. O.; Yang, S. F. Plant Physiol. 1979, 63, 589-590. Yu, Y. B.; Adams, D. O.; Yang, S. F. Arch. Biochem. Biophys. 1979, 198, 280-286. 111. Yang, S. F.; Hoffman, Ν. E. Ann. Rev. Plant Physiol. 1984, 35, 155189. 112. Bailey, J. Α.; Mansfield, J. W., Eds.; Phytoalexins; Blackie: Glasgow, 1982. 113. Kuc, J.; Rush, J. S. Arch. Biochem. Biophys. 1985, 236, 455-472. 114. Pegg, G. F. In Encyclopedia of Plant Physiology; Heitefuss, R., Williams, P. H., Eds.; Springer: Berlin, 1976; New Series Vol. 4, pp 450-479. 115. Elstner, E. F. BIUZ 1978, 8, 82-87. 116. Yang, S. F.; Pratt, Η. K. In Biochemistry of Wounded Plant Tissues; Kahl, G., Ed.; Walter de Gruyter: Berlin, 1978; pp 595-622. 117. DeBlic, Α.; Cazaux, L.; Gorrichon-Guigon, L.; Perry, M. Synthesis 1982, 281, 281-282. 118. Baltas, M.; Bastide, J. D.; Cazaux, L.; Gorrichon-Guigon, L.; Maroni, P.; Tisnes, P. Spectrochim. Acta 1985, 41A, 793-796. 119. Grand, C.; Sarni, F.; Boudet, A. M. Planta 1985, 163, 232-237. 120. Baltas, M.; Cazaux, L.; Gorrichon-Guigon, L.; Maroni, P.; Tisnes, P. Tetrahedron Lett. 1985, 26, 4447-4450. 121. Abeles, R. H.; Maycock, A. L. Acc. Chem. Res. 1976, 9, 313-319. 122. Keen, N. T.; Partridge, J. E.; Zaki, A. J. Phytopathol. 1972, 62, 768. 123. Keen, Ν. T. Science 1975, 187, 74-75. 124. Callow, J. A. In Encyclopedia of Plant Physiology; Linskens, H. F., Heslop-Harrison, J., Eds.; Springer: Berlin, 1984; New Series Vol. 17, pp 212-237. 125. Pearce, R. B.; Ride, J. P. Physiol. Plant Pathol. 1982, 20, 119-123. 126. Barber, M. S.; Ride, J. P. Physiol. Molec. Plant Pathol. 1988, 32, 185197. 127. Kogel, G.; Beiβmann, B.; Reisener, H. J.; Kogel, Κ. H. Physiol. Mol. Plant Pathol. 1988, 33, 173-185. 128. Deverall, B. J.; Deakin, A. L. Physiol. Plant Pathol. 1985, 27, 99-107. 129. Deverall, B. J.; Deakin, A. L. Physiol. Molec. Plant Pathol. 1987, 30, 225-232. 130. Day, P. R. Genetics of Host-Parasite Interaction; W. H. Freeman: San Francisco, 1974. 131. Heath, M. C. Phytopathol. 1981, 71, 1121-1123. 132. Bushnell, W. R., Rowell, J. B. Phytopathol. 1981, 71, 1012-1014. 133. VanSumere, C. F.; VanSumere-DePreter, C.; Ledingham, G. A. Can. J. Microbiol. 1957, 3, 761-770. RECEIVED March 10, 1989


Lignin Biosynthesis in Stem Rust Infected Wheat - ACS Symposium

Recommend Documents