Control of Plant Cell Wall Biogenesis - ACS Symposium Series (ACS

Chapter 1

Control of Plant Cell Wall Biogenesis An Overview D . H . Northcote

Downloaded by 80.82.77.83 on May 1, 2017 | http://pubs.acs.org Publication Date: July 31, 1989 | doi: 10.1021/bk-1989-0399.ch001

Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge CB2 1QW, England

All the polysaccharides of the cell wall are synthesized in association with phospholipid membranes. The hemicelluloses and pectin polysaccharides are formed at the membranes of the Golgi apparatus, cellulose at the plasma membrane. Control of the rate of polysaccharide synthesized and the type of polymer formed is exerted by the transport of donor nucleoside diphosphate sugar molecules across the membranes, the amount, type, and activity of the synthases (glycosyltransferases) and fusion and targetting of vesicles containing the polysaccharides at specific sites at the plasma membrane. The formation of a polysaccharide typically depends on an enzyme complex organized on a membrane. The complex consists of transporters, glycosyltransferases, epimerases and binding proteins to hold the acceptor molecules. In addition to these, subsidiary proteins may also be present which may act to bring about and control the assembly of the complex and its location on the membrane. They may also act as modulators of the polysaccharide synthesis in conjunction with smaller molecules or ions. During xylem formation, lignin is deposited as well as polysaccharides. Part of the control mechanism for the formation of lignin is the level of phenylalanine ammonia lyase activity. Proteins and lipids are also deposited in the wall and although these constituents are not present in large amounts, they are very important for the function of the wall and the cell during growth.

0097-6156/89/0399-0001$06.00/0 © 1989 American Chemical Society

Lewis and Paice; Plant Cell Wall Polymers ACS Symposium Series; American Chemical Society: Washington, DC, 1989.


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

T h e cell w a l l is f o r m e d f r o m m a t e r i a l s w i t h i n the c y t o p l a s m w h i c h are subsequently t r a n s p o r t e d either as m o n o m e r s or p o l y m e r s to the outside of the cell. D u r i n g g r o w t h a n d differentiation of the cell its c o m p o s i t i o n a n d s t r u c t u r e changes, a n d i t can also alter i n response to e n v i r o n m e n t a l factors. T h e r e is therefore a dialogue between the outside of the cell a n d the s y n t h e t i c a n d t r a n s p o r t systems at the inside of the cell so t h a t the changes i n the w a l l are b r o u g h t about i n a n ordered m a n n e r at p a r t i c u l a r stages of its development (1). T h e m a j o r p o l y m e r s t h a t m a k e u p the w a l l are p o l y s a c c h a r i d e s a n d l i g n i n . These o c c u r together w i t h more m i n o r b u t very i m p o r t a n t c o n s t i t u e n t s such as p r o t e i n a n d l i p i d . W a t e r constitutes a m a j o r a n d very i m p o r t a n t m a t e r i a l of y o u n g , p r i m a r y walls (2). T h e l i g n i n is t r a n s p o r t e d i n the f o r m of its b u i l d i n g u n i t s (these m a y be present as glucosides) a n d is p o l y m e r i z e d w i t h i n the w a l l . T h o s e polysaccharides w h i c h make u p the m a t r i x of the w a l l (hemicelluloses a n d p e c t i n m a t e r i a l ) are p o l y m e r i z e d i n the e n d o m e m b r a n e s y s t e m a n d are secreted i n a preformed c o n d i t i o n to the outside of the cell. F u r t h e r m o d i f i c a t i o n s of the polysaccharides (such as a c e t y l a t i o n ) m a y o c c u r w i t h i n the w a l l after d e p o s i t i o n . C e l l u l o s e is p o l y m e r i z e d at the cell surface b y a c o m p l e x e n z y m e s y s t e m t r a n s p o r t e d to the p l a s m a m e m b r a n e (3). T h e c o n t r o l of the development of the cell w a l l m u s t be r e g u l a t e d at the various processes w h i c h m a k e the constituents a n d w h i c h deposits t h e m to the outside of the cell. These m a y be s u m m a r i z e d as follows: (1) r e g u l a t i o n of synthesis b y the a m o u n t s of the synthase; this is d i r e c t l y c o n t r o l l e d by gene r e g u l a t i o n ; (2) b i o c h e m i c a l feed-back c o n t r o l m e c h a n i s m s w h i c h regulate the level of the precursors of the p o l y m e r s or the a c t i v i t i e s of the synthases w h i c h f o r m t h e m ; (3) r e g u l a t i o n of the segregation a n d t a r g e t t i n g of m a t e r i a l f o r m e d w i t h i n the e n d o p l a s m i c r e t i c u l u m a n d G o l g i a p p a r a t u s ; (4) c o n t r o l of t r a n s p o r t of m o n o m e r s to the synthases of the p o l y m e r s ; (5) c o n t r o l of vesicle fusion a n d t a r g e t t i n g of the m e m b r a n e b o u n d m a t e r i a l to specific sites at the cell surface; (6) receptors for p l a n t g r o w t h substances a n d mechanisms for cell s i g n a l l i n g at the c y t o p l a s m i c surface a n d other cell m e m b r a n e s . T h i s chapter reviews some of these topics i n more d e t a i l for the p o l y s a c c h a r i d e s , l i g n i n , p r o t e i n a n d l i p i d of the w a l l . Polysaccharides T h i s section describes a d e t a i l e d hypothesis for the c o n t r o l of p o l y s a c c h a r i d e synthesis a n d d e p o s i t i o n i n the w a l l d u r i n g g r o w t h . M o s t of the b i o c h e m i c a l studies o n p o l y s a c c h a r i d e synthesis to date have been concerned w i t h the f o r m a t i o n of h o m o p o l y m e r s even w h e n it is k n o w n t h a t the synthesis o f the h o m o p o l y m e r c h a i n occurs in vivo as p a r t of a h e t e r o p o l y s a c c h a r i d e (4-6). C y t o c h e m i c a l investigations have m a d e no s u c h d i s t i n c t i o n s a n d the p o l y m e r s located b y these studies have n e a r l y a l ways been sites at w h i c h h e t e r o p o l y m e r s were present a n d where d e p o s i t i o n i n the w a l l o c c u r r e d . T h e b u l k of the polysaccharides t h a t o c c u r i n the w a l l , w i t h the e x c e p t i o n of cellulose a n d callose, are h e t e r o p o l y m e r s . G e n e r a l l y the polysaccharides of the hemicelluloses a n d pectins are c o m p o s e d o f p o l y -



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Control of Plant Cell Wall Biogenesis

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mers c o n t a i n i n g different monosaccharides c o m b i n e d b y different linkages ( 2 , 7 - 1 0 ) . U s u a l l y there is a b a c k b o n e m a d e u p of a single c h a i n , b u i l t o f the same m o n o s a c c h a r i d e (two i n the case o f g l u c o m a n n a n s , see b e l o w ) u s u a l l y c o m b i n e d b y a specific l i n k a g e , o n t o w h i c h short branches are a t t a c h e d w h i c h m a y be j u s t a single monosaccharide different f r o m t h a t of the u n i t s of the m a i n c h a i n , e.g., g l u c u r o n o x y l a n , a r a b i n o g l u c u r o n o x y l a n s , x y l o g l u cans. I n a d d i t i o n more c o m p l i c a t e d p o l y m e r s such as the a r a b i n o g a l a c t a n s o c c u r b u t even i n these p o l y m e r s there is a c e n t r a l core o n t o w h i c h the branches are c o n s t r u c t e d (2). T h e influence of the i n c o r p o r a t i o n of the side branches o n the synthesis of the m a i n c h a i n a n d vice v e r s a is of some significance for the c o n t r o l o f the p o l y s a c c h a r i d e synthesis a n d i n t r o d u c e s the i d e a of a n e n z y m e c o m p l e x at the site for the p o l y m e r s y n t h e s i s . T h e b a c k b o n e c h a i n c a n i n m o s t cases be s y n t h e s i z e d separately w h e n a n in vitro s y s t e m is used. T h e s e investigations have s h o w n t h a t the s y n thase a c t i v i t i e s w h i c h transfer the sugar f r o m a nucleoside d i p h o s p h a t e sugar d o n o r to the g r o w i n g p o l y s a c c h a r i d e c h a i n are r e l a t e d t o the a m o u n t of p o l y s a c c h a r i d e w h i c h is f o r m e d at a n y stage of the g r o w t h a n d developm e n t of the w a l l (5, 6 , 1 1 , 1 2 ) . T h e r e is also s t r o n g c i r c u m s t a n t i a l evidence w h i c h i n d i c a t e s t h a t these v a r i a t i o n s i n a c t i v i t y are due t o changes i n the a m o u n t s of the synthases w h i c h are available at the p a r t i c u l a r sites at a p a r t i c u l a r t i m e (13). T h u s the development o f the w a l l has some c o n t r o l m e c h a n i s m s d i r e c t l y related to the r e g u l a t i o n of the genome d u r i n g diff e r e n t i a t i o n ; t h i s controls the a m o u n t s of the synthases w h i c h are f o r m e d , p r o b a b l y at the level o f t r a n s c r i p t i o n r a t h e r t h a n t r a n s l a t i o n . Synthesis. T h e synthases are present at the e n d o m e m b r a n e s y s t e m o f the cell a n d have been isolated on m e m b r a n e f r a c t i o n s p r e p a r e d f r o m the cells ( 5 , 6 ) . T h e nucleoside d i p h o s p h a t e sugars w h i c h are used b y the synthases are f o r m e d i n the c y t o p l a s m , a n d u s u a l l y the epimerases a n d the other e n zymes (e.g., dehydrogenases a n d decarboxylases) w h i c h i n t e r c o n v e r t t h e m are also soluble a n d p r o b a b l y o c c u r i n the c y t o p l a s m (14). Nevertheless some epimerases are m e m b r a n e b o u n d a n d t h i s m a y be i m p o r t a n t for the r e g u l a t i o n of the synthases w h i c h use the different epimers i n a hete r o p o l y s a c c h a r i d e . T h i s is e s p e c i a l l y significant because the a v a i l a b i l i t y of the d o n o r c o m p o u n d s at the site of the transglycosylases (the synthases) is of obvious i m p o r t a n c e for c o n t r o l of the synthesis. T h e synthases are l o c a t e d at the l u m e n side o f the m e m b r a n e a n d the nucleoside d i p h o s p h a t e sugars m u s t therefore cross the m e m b r a n e i n order to t a k e p a r t i n the rea c t i o n . M o d u l a t i o n o f t h i s t r a n s p o r t m e c h a n i s m is a n o b v i o u s p o i n t for the c o n t r o l not o n l y for the rate of synthesis b u t for the t y p e of synthesis w h i c h occurs i n the p a r t i c u l a r l u m e n of the m e m b r a n e s y s t e m . O b v i o u s l y the s y n t h a s e c a n n o t f u n c t i o n unless the d o n o r m o l e c u l e is t r a n s p o r t e d to its active site a n d the t r a n s p o r t e r s m a y o n l y be present at c e r t a i n regions w i t h i n the e n d o m e m b r a n e s y s t e m . It has been observed t h a t w h e n i n t a c t cells are fed r a d i o a c t i v e monosaccharides w h i c h w i l l f o r m a n d l a b e l p o l y s a c charides, these cannot a l w a y s be f o u n d at a l l the m e m b r a n e sites w i t h i n the cell where the synthase a c t i v i t i e s are k n o w n to o c c u r (15). A p o s s i b l e r e a son for t h i s difference m a y be the selection of precursors b y the t r a n s p o r t mechanism.



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PLANT C E L L W A L L POLYMERS

T h e preformed polysaccharides before they are deposited i n the w a l l can be detected i n the G o l g i a p p a r a t u s either b y r a d i o a c t i v e l a b e l l i n g tech niques a n d direct analysis of the isolated organelle, or b y c y t o c h e m i c a l s t a i n s , the m o s t specific of w h i c h are i d e n t i f i c a t i o n s u s i n g a n t i b o d i e s . F i g ure 1 shows a section of a d e v e l o p i n g secondary w a l l f r o m the h y p o c o t y l cells of b e a n . T h e a n t i b o d y was raised i n r a b b i t s against oligosaccharides prepared f r o m w a l n u t β 1 —• 4 x y l a n (5) a n d conjugated to b o v i n e s e r u m a l b u m i n . T h e a n t i b o d y to the p r o t e i n was removed b y affinity c h r o m a t o g r a p h y a n d the r e s u l t a n t p u r i f i e d a n t i b o d y was specific to antigens c a r r y i n g β 1 —• 4 xylose u n i t s . It d i d not cross-react w i t h x y l o g l u c a n , β 1 —• 4 g l u c a n , a r a b i n a n or m a n n a n . T h e section s h o w n i n F i g u r e 1 was treated w i t h the a n t i b o d y a n d s t a i n e d w i t h g o l d - l a b e l l e d g o a t - a n t i r a b b i t s e r u m . T h e x y l a n is present at the secondary w a l l (st) a n d i n the vesicles of the G o l g i a p p a r a t u s (v). F i g u r e 2 shows a m e r i s t e m a t i c cell f r o m the root of b e a n , treated w i t h an a n t i b o d y specific for L - a r a b i n o f u r a n o s e a n d s t a i n e d w i t h g o l d - l a b e l l e d g o a t - a n t i r a b b i t s e r u m . T h e label was present at the cell w a l l (cw) a n d the developing cell-plate (cp) where p e c t i n was b e i n g l a i d d o w n . Glucomannan Synthesis. A l t h o u g h the heteropolymers are u s u a l l y s i m i l a r to the g l u c u r o n o a r a b i n o x y l a n s , there are heteropolymers i n w h i c h two dif ferent monosaccharides occur i n the m a i n c h a i n , e.g., g l u c o m a n n a n s a n d g a l a c t o g l u c o m a n n a n s . F o r a discussion of the c o n s t r u c t i o n a n d c o n t r o l of the synthesis of a h e t e r o p o l y m e r the synthesis of g l u c o m a n n a n i n the h e m i cellulose of g y m n o s p e r m s serves as a g o o d e x a m p l e ( 1 6 , 1 7 ) . A m e m b r a n e p r e p a r a t i o n isolated f r o m pine s t e m tissues i n c o r p o r a t e d glucose i n t o glucans f r o m b o t h U D P G l c a n d G D P G l c . T h e s e were m i x e d p o l y m e r s c o n t a i n i n g β 1 —• 3 a n d β 1 —> 4 l i n k e d glucose. It also c a r r i e d an epimerase w h i c h interconverted G D P G l c a n d G D P M a n (18). T h e m e m brane p r e p a r a t i o n formed a g l u c o m a n n a n i n the presence of added G D P M a n a n d i n the presence of G D P M a n the f o r m a t i o n of g l u c a n c o n t a i n i n g β 1 —• 3 l i n k s f r o m G D P G l c was repressed a n d the β 1 —• 4 g l u c o m a n n a n was f o r m e d (whether a separate β 1 —*· 4 g l u c a n was synthesized i n a d d i t i o n was difficult to determine) ( T a b l e I) (18). T h e a c t i v i t y of the g l u c a n synthase w h i c h used U D P G l c was unaffected b y the presence of G D P M a n . T h e s e observations c a n best be e x p l a i n e d i n t e r m s of a n e n z y m e c o m p l e x carried o n the m e m b r a n e . T h i s c o m p l e x has a m i n i m u m of three a c t i v i t i e s : (1) a n epimerase for the interconversion of G D P M a n a n d G D P G l c ; (2) a synthase w h i c h used U D P G l c ; (3) a synthase w h i c h used b o t h G D P G l c a n d G D P M a n . T h i s l a t t e r synthase h a d a greater affinity for G D P G l c t h a n G D P M a n a n d , in vitro, i n the presence of G D P G l c b u t i n the a b sence of added G D P M a n , i t formed a g l u c a n i n spite of the presence of the epimerase. Since the influence of the presence-of the G D P M a n o n the i n c o r p o r a t i o n f r o m G D P G l c into a different type of p o l y m e r is so direct, the two a c t i v i t i e s , one for the transfer of glucose a n d the other for the transfer of mannose f r o m the G D P sugars, must either be c a r r i e d out b y the same transglycosylase or the two transglycosylases must be very close together so t h a t they can influence one another.



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S

F i g u r e 1. D e v e l o p i n g secondary thickened w a l l of the h y p o c o t y l of Phaseolus vulgaris. T h e s e c t i o n was treated w i t h a n a n t i b o d y specific for β 1 —• 4 linked D-xylose units and stained w i t h gold-labelled goat-antirabbit serum. T h e l a b e l is seen at the secondary t h i c k e n i n g (st) a n d the vesicles of the G o l g i a p p a r a t u s (v).

F i g u r e 2. M e r i s t e m a t i c cell of the r o o t - t i p of Phaseolus vulgaris. T h e s e c t i o n was treated w i t h a n a n t i b o d y specific for L - a r a b i n o f u r a n o s e a n d s t a i n e d w i t h g o l d - l a b e l l e d g o a t - a n t i r a b b i t s e r u m . T h e l a b e l is seen at the developing cell p l a t e (cp) a n d the y o u n g w a l l (cw) of the m o t h e r c e l l .


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T a b l e I. T h e influence of the presence of exogenous G D P M a n o n the s y n thesis of a m i x e d βΐ —• 3, 1 —• 4 g l u c a n f r o m G D P G l c b y a m e m b r a n e p r e p a r a t i o n f r o m pine s t e m tissue. M e a s u r e m e n t s were m a d e f r o m the i n c o r p o r a t i o n of r a d i o a c t i v e glucose f r o m G D P [ U C ] G l c (18). (- indicates t h a t no g l u c a n c a r r y i n g a βΐ —• 3 linkage was formed.) 1 4

G D P [ U - C ] G l c as the P r i m a r y S u b s t r a t e (1.0 n m o l ) 1 4

GDPMan Additions nmol

βΐ —• 3,1 —» 4 g l u c a n formed nmol. m i n " (mg p r o t e i n ) " 1


1

0.0 0.5 1.0 2.5 5.0 10.0

0.28 -

β! —» 4 g l u c o m a n n a n formed nmol. m i n " ( m g protein) 0.0 0.57 0.56 1.0 0.70 0.39

It is likely t h a t i n a d d i t i o n to the synthases a n d epimerases there is also present at the m e m b r a n e i n close p r o x i m i t y to these, t r a n s p o r t e r systems for the transfer of the nucleoside d i p h o s p h a t e donor c o m p o u n d s t o the transglycosylases s i t u a t e d o n the l u m e n side of the m e m b r a n e . T h e p o l y m e r w h i c h formed was either a m i x e d /? 1 —• 3, β I —• 4 g l u c a n or a β 1 —* 4 g l u c o m a n n a n a n d runs of β 1 —• 4 l i n k e d glucose o c c u r r e d i n the g l u c o m a n n a n (18). T h e g l u c o s y l transferase t h a t used G D P G l c added glucose either at the 3 p o s i t i o n of the r e c e i v i n g sugar, or at the 4 p o s i t i o n . It was also s h o w n t h a t the transglucosylase added the g l u c o s y l r a d i c a l to water to f o r m free glucose (18). In t h i s s y s t e m , therefore, the transglycosylase u s i n g G D P G l c was not specific for the receptor molecule since t h i s m a y be w a t e r , glucose at the 3 p o s i t i o n , glucose at the 4 p o s i t i o n , or m a n n o s e at the 4 p o s i t i o n . W h e n a g l u c o m a n n a n was f o r m e d , the linkage was a l w a y s m a d e at the 4 p o s i t i o n . T h e acceptor molecule, a l t h o u g h i t was not specific i n the t r a n s g l y c o s y l r e a c t i o n , influenced h o w the transfer o c c u r r e d . T h e s e diverse actions of the transglycosylase c a n be most easily ex p l a i n e d b y p o s t u l a t i n g the existence of a b i n d i n g p r o t e i n w h i c h holds the acceptor molecules. T h e n d u r i n g the transglycosylase r e a c t i o n t h a t forms the g l u c o m a n n a n c h a i n , a g l u c o s y l r a d i c a l c o u l d first be transferred to w a ter w i t h i n an associated b i n d i n g p r o t e i n a n d the r e s u l t a n t sugar c o u l d t h e n be e x t e n d e d b y subsequent transfers to the n o n - r e d u c i n g end of the g r o w i n g c h a i n , either f r o m G D P M a n or G D P G l c . It is possible to have the acceptor sugar precisely o r i e n t a t e d b y such a b i n d i n g p r o t e i n , i n order to receive the new g l y c o s y l residue b y the transglycosylase at the p a r t i c u l a r h y d r o x y l w h i c h is presented to the d o n o r molecule. T h e transglycosylase i t s e l f c o u l d have a d o m a i n at w h i c h the acceptor oligosaccharide was h e l d b u t since the


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o r i e n t a t i o n of the acceptor m o l e c u l e is altered i n d e p e n d e n t l y of the t r a n s glycosylase there are p r o b a b l y at least t w o p r o t e i n s i n v o l v e d : one used for transfer a n d h o l d i n g the donor a n d another necessary for h o l d i n g the accept o r . T h e transglycosylase p r o t e i n is not therefore specific for the acceptor m o l e c u l e . T h i s is i n contrast to the way i n w h i c h the g l y c o s y l a t i o n of cert a i n g l y c o p r o t e i n s is t h o u g h t to occur (19). D e f i n i t e sequences of sugars are b u i l t o n the p r o t e i n because the various transglycosylases i n v o l v e d are specific for the acceptor oligosaccharide w h i c h changes i n a stepwise m a n ner. A t each stage a definite glycosyltransferase c a n act t o f o r m a definite sequence of sugars. Binding Protein and Enzyme Complex. T h a t sugars a n d oligosaccharides c a n s p e c i f i c a l l y b i n d t o p r o t e i n is w e l l k n o w n . H e x o k i n a s e is k n o w n to h o l d glucose w i t h i n a cleft of the e n z y m e b y h y d r o g e n b o n d s ; i n d e e d , the presence of glucose causes a m o v e m e n t i n the c o n f o r m a t i o n a l s t r u c t u r e o f the p r o t e i n so t h a t i t folds a r o u n d the glucose a n d the h y d r o x y l g r o u p a t the 6 p o s i t i o n is presented to the kinase for the transfer of the p h o s p h a t e g r o u p f r o m the A T P (20). Specific associations between proteins a n d o l i g o s a c c h a rides a n d polysaccharides are also w e l l d o c u m e n t e d . L y s o z y m e a n d t a k a amylase are k n o w n to h o l d oligosaccharides i n a r i b b o n - l i k e c o n f i g u r a t i o n b y h y d r o g e n b o n d i n g a n d v a n der W a a l s forces w i t h i n a b i n d i n g - s i t e groove (21). Precise a n d stereospecific i n t e r a c t i o n s are f o r m e d a n d m a i n t a i n e d b y the o r i e n t a t i o n o f h y d r o g e n - b o n d i n g residues w h i c h are i n t u r n fixed b y c o m p l e x h y d r o g e n b o n d networks to other residues w i t h i n the b i n d i n g sites. D u r i n g b i n d i n g , c o n f o r m a t i o n a l changes m a y o c c u r w h i c h allow the c a r b o h y d r a t e s to be o r i e n t e d for the b i n d i n g to progress a n d specific i n t e r a c t i o n between p r o t e i n a n d c a r b o h y d r a t e results (22). D u r i n g the synthesis of a m i x e d p o l y s a c c h a r i d e s u c h as a g l u c u r o n o x y l a n or a x y l o g l u c a n , at least two transglycosylases are i n v o l v e d w h i c h w o r k i n c o n j u n c t i o n w i t h one another (23-27). It is possible to envisage the m a i n c h a i n of either glucose or x y l o s e b e i n g h e l d b y a b i n d i n g p r o t e i n a n d the side chains being g u i d e d o n t o the b a c k b o n e w h i c h is h e l d i n such a w a y as t o present the a p p r o p r i a t e h y d r o x y l to the s u b s t i t u e n t sugar a n d the appropriate transglycosylase. W h a t e v e r the m e c h a n i s m , the c o o r d i n a t e d synthesis of a p o l y s a c c h a r i d e , s u c h as g l u c o m a n n a n or g l u c u r o n o x y l a n or the a r a b i n o g a l a c t a n s of the p e c t i n s or even a h o m o p o l y m e r s u c h as single cellulose c h a i n s (3), needs the c o o p e r a t i o n of a set of p r o t e i n s . These m u s t be o r g a n i z e d close to one a n other i n correct o r i e n t a t i o n for the synthesis t o o c c u r i n a n e c o n o m i c a l a n d r a p i d m a n n e r . T h e r e is t h u s a m u l t i e n z y m e s y s t e m o r g a n i z e d o n the m e m brane a n d h e l d i n a c o o r d i n a t e d way. T h e m e m b r a n e o n a n d i n w h i c h the p r o t e i n s are h e l d becomes a n i m p o r t a n t p a r t of the s y n t h e t i c process. D i s r u p t i o n o f the m e m b r a n e w i l l b r i n g a b o u t loss o f o r g a n i z a t i o n a n d the in vitro p r e p a r a t i o n s m a d e f r o m i n t a c t cells m a y f o r m p o l y s a c c h a r i d e s different f r o m those f o r m e d in vivo (e.g., callose i n s t e a d of cellulose) (28) or for a h e t e r o p o l y s a c c h a r i d e the dependence of one t r a n s g l y c o s y l a s e o n the a c t i o n o f a n o t h e r w i l l b e c o m e less precise ( 2 4 , 2 9 ) i n the in vitro p r e p a r a t i o n t h a n i n the i n t a c t cell.


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It seems likely t h a t the e n z y m e complexes for hemicelluloses, pectins a n d cellulose are c o n s t r u c t e d , at least i n p a r t , o n the e n d o p l a s m i c r e t i c u l u m a n d then transferred to the G o l g i a p p a r a t u s , where they are m o d i f i e d a n d sorted so t h a t they can be segregated w i t h i n the c o m p a r t m e n t s of the G o l g i cisternae ( 3 0 , 3 1 ) . T h e c o m p l e x for cellulose synthesis is not n o r m a l l y a c t i v e w i t h i n the G o l g i a p p a r a t u s a n d i t is t r a n s p o r t e d to active sites at the p l a s m a m e m b r a n e (1). T h e hemicelluloses a n d pectins are f o r m e d w i t h i n vesicles a n d cisternae of the G o l g i a p p a r a t u s a n d the vesicles are t r a n s p o r t e d to the p l a s m a m e m b r a n e , where fusion occurs a n d the polysaccharides are packed i n t o the w a l l (1). It is not k n o w n whether p a r t i c u l a r polysaccharides such as the x y l a n s of the hemicellulose a n d the a r a b i n o g a l a c t a n s of the p e c t i n s are t r a n s p o r t e d i n separate vesicles or together i n one vesicle. N o r is i t k n o w n i f the c o m p l e x for cellulose synthesis is t r a n s p o r t e d by vesicles w h i c h c a r r y hemicellulose a n d p e c t i n polysaccharides. Deposition of Wall Polysaccharides. W h a t e v e r the d i s t r i b u t i o n of the polysaccharides a n d synthase systems i n the vesicles, the movement of the vesicles to p a r t i c u l a r sites a n d the rate of fusion w i t h the p l a s m a m e m b r a n e c o n s t i t u t e i m p o r t a n t c o n t r o l p o i n t s for the d e p o s i t i o n of the m a t e r i a l i n t o the w a l l . It is k n o w n t h a t at sites of active w a l l d e p o s i t i o n vesicles are d i rected to the p l a s m a m e m b r a n e b y m i c r o t u b u l e s (32). However, i t is possible t h a t other signals a n d receptors at the m e m b r a n e surface m a y be i n v o l v e d i n r e c o g n i t i o n of the sites for i n c o r p o r a t i o n . P a r t of the c o n t r o l for vesicle fusion at the surface is m e d i a t e d by the i o n i c atmosphere at the m e m b r a n e , and C a is necessary for the fusion to o c c u r . T h e rate of vesicle fusion can be a l i m i t i n g process for the rate of cell w a l l f o r m a t i o n , since at a n y one t i m e the n u m b e r of vesicles ready for fusion exceeds the n u m b e r t h a t are f u s i n g a n d d e p o s i t i n g m a t e r i a l into the w a l l . In t h i s way the c o m p o s i t i o n a n d a m o u n t of w a l l m a t e r i a l deposited m a y respond very q u i c k l y to a s t i m u l u s at the cell surface w h i c h allows the rate of vesicle fusion to vary. For instance, the m a t e r i a l deposited i n the cell w a l l , especially the p e c t i n , changes very q u i c k l y at the i n i t i a l stages of p l a s m o l y s i s w h e n the w a l l is j u s t separated f r o m the p l a s m a m e m b r a n e . A new steady state w o u l d t h e n be achieved t h a t p r o d u c e d the requisite n u m b e r of vesicles f r o m the G o l g i a p p a r a t u s to m a i n t a i n the altered rate of fusion (32-34). 2 +

Lignin Precursors and Lignin Formation Phenylalanine Ammonia-Lyase. T h e b u i l d i n g u n i t s of l i g n i n are f o r m e d f r o m c a r b o h y d r a t e v i a the s h i k i m i c a c i d p a t h w a y to give a r o m a t i c a m i n o acids. Once the a r o m a t i c a m i n o acids are f o r m e d , a key e n z y m e for the c o n t r o l of l i g n i n precursor synthesis is 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 ) (1). T h i s e n z y m e catalyzes the p r o d u c t i o n of c i n n a m i c a c i d f r o m p h e n y l a l a n i n e . It is very active i n those tissues of the plant t h a t become lignified a n d it is also a c e n t r a l enzyme for the p r o d u c t i o n of other p h e n y l p r o p a n o i d d e r i v e d c o m p o u n d s such as flavonoids a n d c o u m a r i n s , w h i c h can o c c u r i n m a n y p a r t s of the plant a n d i n m a n y different organs (35). R a d i o a c t i v e p h e n y l a l a n i n e a n d c i n n a m i c a c i d are d i r e c t l y i n c o r p o r a t e d i n t o l i g n i n i n vascular tissue (36).



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T h e i n d u c t i o n o f P A L a c t i v i t y at the onset o f vascular d i f f e r e n t i a t i o n c a n be s h o w n b y the use o f p l a n t tissue c u l t u r e s (37-39). X y l e m cells w i t h secondary a n d l i g n i f i e d w a l l s are differentiated over a t i m e course o f 3-14 d a y s b y the a p p l i c a t i o n of the p l a n t g r o w t h factors n a p h t h y l e n e acetic a c i d ( N A A ) a n d k i n e t i n i n the r a t i o 5:1 (1.0 m g / l i t e r N A A , 0.2 m g / l i t e r k i n e t i n ) to tissue cultures of b e a n cells (Phaseolus vulgaris) ( 3 7 , 4 0 ) . T h e t i m e for d i f f e r e n t i a t i o n varies w i t h the t y p e of c u l t u r e , s o l i d or s u s p e n s i o n , a n d w i t h the frequency a n d d u r a t i o n of s u b c u l t u r e , b u t for a n y one c u l t u r e i t is r e l a t i v e l y constant ( 3 7 , 4 1 , 4 2 ) . A t the t i m e of d i f f e r e n t i a t i o n w h e n the x y l e m vessels f o r m , the a c t i v i t y of P A L rises to a m a x i m u m . T h e r i s i n g phase of the e n z y m e a c t i v i t y was i n h i b i t e d b y a c t i n o m y c i n D a n d b y D - 2 , 4 - ( 4 methyl-2,6-dinitroanilino)-N-methylpropionamide ( M D M P ) applied under c a r e f u l l y c o n t r o l l e d c o n d i t i o n s (42). T h i s i n d i c a t e d t h a t b o t h t r a n s c r i p t i o n a n d t r a n s l a t i o n were necessary for the response to the h o r m o n e s . E x p e r i m e n t s u s i n g a n a n t i b o d y for P A L a n d a c D N A p r o b e for the P A L - m R N A have also s h o w n t h a t there is a n increase i n the a m o u n t of t r a n s c r i p t for P A L d u r i n g the f o r m a t i o n of l i g n i n w h e n Z i n n i a m e s o p h y l l cells are i n d u c e d to f o r m x y l e m elements i n c u l t u r e ( L i n a n d N o r t h c o t e , u n p u b l i s h e d w o r k ) . T h e i n d u c t i o n of P A L a c t i v i t y b y the two g r o w t h factors can be sepa r a t e d i n t i m e so t h a t they m a y act at different sites w i t h i n the cell to b r i n g a b o u t the response (40). A u x i n a d d e d at the t i m e of s u b c u l t u r e of the tissue changes the p a t t e r n of p r o t e i n synthesis of the cells b y c h a n g i n g the t r a n s c r i p t i o n p a t t e r n of the m R N A after two hours (43). K i n e t i n does not have t h i s effect (44). Hydroxylation and Methylation. T h e p a t h w a y for the p r o d u c t i o n of the l i g n i n b u i l d i n g u n i t s involves h y d r o x y l a t i o n of the a r o m a t i c r i n g a n d m e t h y l a t i o n of the h y d r o x y l groups. It has been d e m o n s t r a t e d t h a t the m e t h y l a t i o n s are b r o u g h t a b o u t by S-adenosylmethionine:caffeic a c i d , 3 - 0 - m e t h y l transferase. T h i s transferase is m e t a specific a n d can also m e t h y l a t e 5h y d r o x y f e r u l i c a c i d a n d 3 , 4 , 5 - t r i h y d r o x y c i n n a m i c a c i d t o s i n a p i c a c i d (45). T h e i n d u c t i o n o f t h i s e n z y m e i n b e a n cultures d u r i n g d i f f e r e n t i a t i o n is c o i n cident w i t h the rise i n P A L a c t i v i t y (46). T h e h y d r o x y l a t i o n o f the a r o m a t i c r i n g o f c i n n a m i c a c i d is b r o u g h t a b o u t b y c i n n a m i c a c i d 4 - h y d r o x y l a s e , a n d a f u r t h e r h y d r o x y l a s e , p - c o u m a r i c a c i d 3 - h y d r o x y l a s e , also o c c u r s t o give caffeic a c i d (47). T h e 4 - h y d r o x y l a s e a c t i v i t y , i n some tissue, is i n d u c e d at the same t i m e as the P A L a c t i v i t y ( 4 8 , 4 9 ) . T h e r e f o r e , some c o o r d i n a t e d i n d u c t i o n of gene expression for the p r o d u c t i o n of l i g n i n precursors d u r i n g d i f f e r e n t i a t i o n is possible. T h e P A L a c t i v i t y t h a t is necessary for l i g n i n f o r m a t i o n o c c u r s i n the c y t o p l a s m or b o u n d to the c y t o p l a s m i c surface of the e n d o p l a s m i c r e t i c u l u m m e m b r a n e s . T h e c i n n a m i c a c i d p r o d u c e d is p r o b a b l y c a r r i e d o n the l i p i d surface of the m e m b r a n e s , since i t is l i p o p h i l i c , a n d i t is s e q u e n t i a l l y h y d r o x y l a t e d b y the m e m b r a n e - b o u n d h y d r o x y l a s e s ( 4 7 , 5 0 ) . I n t h i s w a y there is the p o s s i b i l i t y of at least a two-step c h a n n e l i n g route f r o m p h e n y l a l a n i n e to p - c o u m a r i c a c i d . T h e t r a n s m e t h y l a s e s t h e n direct the m e t h y l groups to the m e t a p o s i t i o n s . T h e r e is a difference between the t r a n s m e t h y lases f r o m a n g i o s p e r m s a n d those f r o m g y m n o s p e r m s , since w i t h the l a t t e r


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p r e p a r a t i o n s the e n z y m e is relative i n a c t i v e o n 5 - h y d r o x y f e r u l a t e . T h u s i t is possible t h a t these t r a n s m e t h y l a s e s m a y have some p a r t i n the c o n t r o l of the t y p e of l i g n i n f o r m e d . T h e g u a i a c y l t y p e ( 3 - m e t h o x y - 4 - h y d r o x y ) is f o u n d i n g y m n o s p e r m s a n d the s y r i n g y l - g u a i a c y l t y p e ( 3 , 5 - d i m e t h o x y - 4 h y d r o x y ) i n dicotyledons (51). Formation and Polymerization of the Building Units of Lignin. T h e acid b u i l d i n g u n i t s are reduced t o the c o r r e s p o n d i n g alcohols before p o l y m e r i z a t i o n t o l i g n i n . T h i s r e d u c t i o n occurs as a two-step process i n v o l v i n g the C o A ester o f the a c i d a n d u s i n g N A D P H as cofactor. T h e enzymes C o A ligase, c i n n a m o y l - C o A : N A D P H oxidoreductase, a n d c i n n a m y l a l c o h o l dehydrogenase are i n v o l v e d , a n d they give f i n a l l y the three b u i l d i n g u n i t s of l i g n i n : p - c o u m a r y l a l c o h o l , c o n i f e r y l a l c o h o l , a n d s i n a p y l a l c o h o l (51). V a r i o u s isoenzymes o f the C o A ligases m a y also c o n t r o l the t y p e o f l i g n i n t h a t is f o r m e d , since the isoenzymes have different affinities a n d a c t i v i t i e s for p - c o u m a r i c , ferulic a n d s i n a p i c a c i d a n d these isoenzymes o c c u r i n different p r o p o r t i o n s i n different p l a n t s a n d i n different tissues o f the same p l a n t (51). T h e a c t i v a t i o n o f the p h e n y l p r o p i o n i c acids a n d t h e i r subsequent red u c t i o n m a y o c c u r i n vesicles t h a t fuse w i t h the p l a s m a m e m b r a n e a n d e m p t y the precursors of l i g n i n i n t o the w a l l (52). T h e N A D P H for the r e d u c t i o n is p r o v i d e d b y the pentose p h o s p h a t e p a t h w a y ( 5 3 , 5 4 ) . T h e c o n t r o l for the f i n a l steps t h a t p r o d u c e the c i n n a m y l alcohols, w h i c h are the i m m e d i a t e b u i l d i n g u n i t s of the l i g n i n , is therefore dependent o n the e n ergy s t a t u s o f the cell, since A T P is necessary for the ligase a c t i v i t y , a n d i t is also dependent o n the d i s t r i b u t i o n of c a r b o h y d r a t e m e t a b o l i s m between the pentose phosphate p a t h w a y a n d g l y c o l y s i s . It is w i t h i n the w a l l t h a t the p o l y m e r i z a t i o n process to f o r m a c o m p l e x l i g n i n cage occurs. T h e c i n n a m y l alcohols m a y reach the w a l l as the free alcohols or as /?-glucosides f o r m e d by glucosyltransferases w i t h U D P G l c (55). F o r p o l y m e r i z a t i o n , the free a l c o h o l is necessary, a n d /?-glucosidases o c c u r i n the walls of tissues t h a t are lignified (56). G l u c o s i d e s m a y be i m p o r t a n t for the t r a n s p o r t of the alcohols t o the w a l l s , b u t they are not o b l i g a t o r y for l i g n i n s y n t h e s i s . T h e y m a y act as reservoirs o f the l i g n i n precursors. T h e p r e c u r sors arise i n cells t h a t are u n d e r g o i n g l i g n i f i c a t i o n , or t h e y m a y arise f r o m n e i g h b o r i n g cells of y o u n g d i f f e r e n t i a t i n g x y l e m , w h i c h themselves are not at the stage o f m a s s i v e l i g n i f i c a t i o n (36). L i g n i f i c a t i o n is b r o u g h t a b o u t b y the o x i d a t i o n of the alcohols to y i e l d mesomeric p h e n o x y r a d i c a l s w i t h h a l f lives of a b o u t 45 sec, so t h a t r a p i d p o l y m e r i z a t i o n occurs. A t the same t i m e , linkages of these r a d i c a l s , a n d hence the l i g n i n , to c a r b o h y d r a t e c a n t a k e place ( 5 6 , 5 7 ) . It is p r o b a b l e t h a t the final o x i d a t i o n of the p h e n o l i c h y d r o x y g r o u p to give the free r a d i c a l s is b r o u g h t a b o u t b y a specific i s o e n z y m e of peroxidase t h a t occurs i n the walls of p l a n t cells (58-60). T h i s i s o e n z y m e , o n electrophoresis, is a n a n o d i c - m i g r a t i n g c o m p o n e n t . I n Zinnia elegans, the a c t i v i t y of w a l l - b o u n d peroxidase increases d u r i n g the onset o f l i g n i f i c a t i o n , a l t h o u g h the t o t a l soluble peroxidase a c t i v i t y of the cell m a y decrease ( 3 9 , 4 6 ) . A n o t h e r i s o e n z y m e of peroxidase m i g h t be r e q u i r e d t o p r o d u c e the h y d r o g e n peroxide o n w h i c h the o x i d a t i v e p o l y m e r i z a t i o n process de-


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p e n d s (61). T h e synthesis a n d a c t i v i t y of some isoenzymes of peroxidase are therefore possible c o n t r o l sites for l i g n i f i c a t i o n . Establishment of Cross Linkages in the W a l l


I n the r i g i d s e c o n d a r y w a l l o f w o o d y tissue, the l i g n i n replaces the water of the g r o w i n g cell w a l l a n d f o r m s a h y d r o p h o b i c m a t r i x a r o u n d the m i crofibrils. S t r o n g h y d r o g e n b o n d s o c c u r between the p o l y s a c c h a r i d e s at the m i c r o f i b r i l l a r - m a t r i x interface a n d between c o m p o n e n t s of the m a t r i x . T h e s e , together w i t h the covalent b o n d s f o r m e d between c a r b o h y d r a t e a n d l i g n i n , m a k e the w a l l a composite i n w h i c h the l i n e a r p o l y s a c c h a r i d e p o l y mers are enclosed i n a c r o s s - l i n k e d p o l y m e r cage. T h e w a l l has great tensile s t r e n g t h because of the m i c r o f i b r i l s a n d a r i g i d s t r u c t u r e because o f the l i g nified m a t r i x (2). T h e peroxidase of the w a l l m a y also e s t a b l i s h other covalent linkages between w a l l p o l y m e r s . T h e w a l l contains p r o t e i n a n d the t y r o s i n e residues of the p r o t e i n s m a y be o x i d i z e d b y peroxidase to give cross-linkages of i s o d i t y r o s i n e between the p o l y p e p t i d e s ( 6 2 , 6 3 ) . F e r u l i c a c i d occurs i n the cell w a l l s of some herbaceous p l a n t s a n d grasses a n d t h i s m a y be o x i d i z e d t o give d i f e r u l i c a c i d ester linkages j o i n i n g p o l y s a c c h a r i d e c h a i n s ( 6 4 , 6 5 ) . T h e possible f o r m a t i o n of these covalent cross linkages between the p o l y m e r s of the p r i m a r y w a l l is believed b y some workers to l i m i t p l a n t cell w a l l e x t e n s i b i l i t y a n d have some p a r t i n the m e c h a n i s m s for the c o n t r o l of cell g r o w t h a n d e x t e n s i o n b y p l a n t g r o w t h factors (66). P r o t e i n i n the W a l l M o s t of the p r o t e i n s f o u n d i n the cell w a l l are g l y c o p r o t e i n s . T h e s e c a n be enzymes s u c h as isoenzymes of peroxidase, phosphatase a n d a m y l a s e or the h y d r o x y p r o l i n e - r i c h g l y c o p r o t e i n s (67) a n d g l y c i n e - r i c h p r o t e i n s (68). T h e h y d r o x y p r o l i n e - r i c h g l y c o p r o t e i n s m a y be classified o n the basis o f the size of t h e i r sugar p r o s t h e t i c groups. T h e soluble lectins a n d a g g l u t i n i n s a n d the i n s o l u b l e w a l l g l y c o p r o t e i n s have s m a l l oligosaccharides of arabinose ( a L - A r a f ( l -+ 3 ) - 0 - / ? - L - A r a f (1 -+ 2 ) - 0 - / ? - L - A r a f ( l - » 2 ) - 0 - / ? - L - A r a f - l H y p ) l i n k e d to the h y d r o x y p r o l i n e ( H y p ) a n d also single galactose u n i t s a t t a c h e d to serine (69-71), w h i l e the a r a b i n o g a l a c t a n p r o t e i n s are m a i n l y large m o l e c u l a r weight p o l y s a c c h a r i d e s a t t a c h e d to p r o t e i n , the r e s u l t a n t m o l e c u l e b e i n g a b o u t 8 0 - 9 0 % c a r b o h y d r a t e ( 7 2 , 7 3 ) . H y d r o x y l a t i o n of p e p t i d y l p r o l i n e o c c u r s as a p o s t - t r a n s l a t i o n a l process i n the e n d o p l a s m i c r e t i c u l u m (74-76), a n d the a d d i t i o n of the s m a l l a r a b i n o s y l oligosaccharides p r o b a b l y occurs w i t h i n the G o l g i a p p a r a t u s w i t h o u t the necessity for a s s e m b l y o n a l i p i d i n t e r m e d i a t e (77). H o w e v e r , w i t h the large m o l e c u l a r weight a r a b i n o g a l a c t a n p r o t e i n a l i p i d c a r r i e r m i g h t be i n v o l v e d , e s p e c i a l l y as r e p e a t i n g s u b u n i t s w i t h i n the a r a b i n o g a l a c t a n p o r t i o n of the m o l e c u l e have been d e t e c t e d . O l i g o s a c c h a r i d e s l i n k e d to p o l y i s o p r e n y l - p y r o p h o s p h a t e have been f o u n d to c o n t a i n arabinose (78) a n d galactose (79); the galactose was l i n k e d b y 1 —• 6, 1 —+ 4 a n d 1 —• 3 bonds a n d the arabinose was 1 —• 5 l i n k e d . T h e s e i s o p r e n y l d i p h o s p h a t e oligosaccharides were f o r m e d b y m e m b r a n e s of p e a



12


cells w h e n they were i n c u b a t e d w i t h the a p p r o p r i a t e r a d i o a c t i v e U D P sugar c o m p o u n d s , a n d they c o u l d serve as precursors of the a r a b i n o g a l a c t a n glycoproteins. T h e possible i n c l u s i o n of l i p i d - l i n k e d intermediates i n the t r a n s g l y c o s y l a t i o n s i n v o l v e d i n g l y c o p r o t e i n a n d p o l y s a c c h a r i d e f o r m a t i o n provides a f u r t h e r step at w h i c h c o n t r o l of the synthase s y s t e m c a n be exercised. H o w e v e r , a l t h o u g h l i p i d intermediates are w e l l established for the f o r m a t i o n of N - l i n k e d glycoproteins a n d , i n some instances, for polysaccharides where g l y c o p r o t e i n s can f u n c t i o n as i n t e r m e d i a t e s d u r i n g the f o r m a t i o n of these polysaccharides (80-82), there is, at present, no evidence for the direct transfer f r o m l i p i d - o l i g o s a c c h a r i d e onto p o l y s a c c h a r i d e . O n e of the i m p o r t a n t consequences of the p a r t i c i p a t i o n of l i p i d - o l i g o s a c c h a r i d e i n t e r m e d i a t e s is t h a t the sequence of sugars f o r m e d on the l i p i d can be successively t r a n s ferred so t h a t a r e p e a t i n g ordered sequence of the m i x e d sugars i n the oligosaccharide c o u l d o c c u r i n the synthesized p o l y m e r (83-85). F o r m a t i o n of L i p i d a n d T r a n s p o r t to the W a l l M a n y cell walls have layers i n the outer regions of the w a l l t h a t c a r r y l i p i d m a t e r i a l . These are c u t i n , s u b e r i n , a n d waxes (67). H o w these are t r a n s p o r t e d to the outside of the cell w a l l is not k n o w n . Pores have not been f o u n d , nor has a v o l a t i l e l i p i d solvent been detected t h a t w o u l d c a r r y the l i p i d t h r o u g h the h y d r o p h i l i c w a l l . T h e f a t t y acids are synthesized i n chloroplasts or p r o p l a s t i d s a n d m o v e d into the c y t o p l a s m a n d the e n d o m e m b r a n e s y s t e m for further m o d i f i c a t i o n a n d synthesis of n e u t r a l fats, p h o s p h o l i p i d s , a n d other c o m p o u n d s (86). T h e f a t t y acids c o u l d be carried b y proteins b y a process s i m i l a r to the way i n w h i c h s e r u m a l b u m i n binds f a t t y a c i d i n the b l o o d s t r e a m of m a m m a l s . O t h e r types of l i p i d m i g h t be f o r m e d i n t o complexes analogous to l o w - d e n s i t y l i p o p r o t e i n s of the type f o u n d i n a n i m a l tissues, where the l i p i d core of the l i p o p r o t e i n is s u r r o u n d e d b y a h y d r o p h i l i c cortex m a d e up of p r o t e i n , p h o s p h o l i p i d , a n d cholesterol (87). T h i s allows the l i p i d to be m o v e d i n an aqueous e n v i r o n m e n t . T h e p r o t e i n of the l i p o p r o t e i n shell c o u l d also act as possible ligands for p a r t i c u l a r receptors at the m e m brane of the cell at w h i c h the e x p o r t occurs. T h e l i p o p r o t e i n s , i f they are present, w o u l d p r o b a b l y be formed w i t h i n the e n d o m e m b r a n e l u m e n a n d w o u l d receive the proteins at the e n d o p l a s m i c r e t i c u l u m . Summary T h i s chapter has a t t e m p t e d to suggest how the synthesis of the m a i n c o n s t i t u e n t s of the w a l l (polysaccharides, l i g n i n , p r o t e i n a n d l i p i d ) are c o n t r o l l e d d u r i n g their d e p o s i t i o n i n t o the w a l l . A hypothesis is developed for the synthesis of polysaccharides. It arises f r o m the evidence for g l u c o m a n n a n synthesis (18), a n d also for cellulose a n d callose synthesis (28). D i f ferent g l y c o s i d i c linkages are f o r m e d f r o m the same m e m b r a n e p r e p a r a t i o n under different c o n d i t i o n s . T h i s is most easily e x p l a i n e d by p o s t u l a t i n g the existence of a b i n d i n g p r o t e i n to h o l d the acceptor molecules of the


1.

NORTHCOTE


13

t r a n s g l y c o s y l a s e r e a c t i o n . T h e hypothesis suggests t h a t there is a c o m p l e x o f p r o t e i n s , w i t h different f u n c t i o n s , o r g a n i z e d close together a t t h e m e m b r a n e o f t h e cell. A t r a n s g l y c o s y l a s e , nucleoside d i p h o s p h a t e sugar t r a n s p o r t e r s , a n d t h e b i n d i n g p r o t e i n are a l l necessary. T h e l a t t e r p r o t e i n , since i t h o l d s the g r o w i n g p o l y s a c c h a r i d e c h a i n , c a n m o d u l a t e t h e t r a n s g l y cosylase r e a c t i o n b y o r i e n t a t i n g the receptor m o l e c u l e . I n t h i s w a y t h e same transglycosylase m a y transfer t h e g l y c o s y l g r o u p t o different h y d r o x y l s o f the acceptor, e.g., t o give 1 —• 3 o r 1 —• 4 linkages.


Literature Cited

1. Northcote, D. H. In Biosynthesis and Biodegradation of Wood Compo nents; Academic Press: London, 1985; Ch. 5. 2. Northcote, D. H. Ann. Rev. Plant Physiol. 1972, 23, 113-132. 3. Northcote, D. H. In Biosynthesis and Biodegradation of Cellulose and Cellulose Materials; Marcel Dekker Inc.: New York, 1988; Ch. 3. 4. Bailey, R. W.; Hassid, W. Z. Proc. Natl. Acad. Sci. 1966, 56, 1586-93. 5. Dalessandro, G.; Northcote, D. H. Planta 1981, 151, 53-60. 6. Dalessandro, G.; Northcote, D. H. Planta 1981, 151, 61-67. 7. Timell, T. E. Adv. Carbohydr. Chem. 1964, 19, 247-302. 8. Timell, T. E. Adv. Carbohydr. Chem. 1965, 20, 409-483. 9. O'Neill, Μ. Α.; Selvendran, R. R. Carb. Res. 1983, 111, 239-255. 10. Aspinall, G. O.; Molloy, J. Α.; Craig, J. W. T. Can. J. Biochem. Phys iol. 1969, 47, 1063-70. 11. Bolwell, G. P.; Northcote, D. H. Planta 1981, 152, 225-33. 12. Bolwell, G. P.; Dalessandro, G.; Northcote, D. H. Phytochem. 1985, 24, 699-702. 13. Bolwell, G. P.; Northcote, D. H. Planta 1984, 162, 139-46. 14. Dalessandro, G.; Northcote, D. H. Biochem. J. 1977, 162, 139-46. 15. Bolwell, G. P.; Northcote, D. H. Biochem. J. 1983, 210, 497-507. 16. Ramsden, L.; Northcote, D. H. Phytochem. 1987, 26, 2679-83. 17. Dalessandro, G.; Piro, G.; Northcote, D. H. Planta 1986, 169, 564-74. 18. Dalessandro, G.; Piro, G.; Northcote, D. H. Planta 1988, 175, 60-70. 19. Watkins, W. M. Carbohydr. Res. 1986, 149, 1-12. 20. Steitz, Τ. Α.; Shoham, M.; Bennett, W. S. Phil. Trans. R. Soc. London 1981, B293, 43-52. 21. Matsura, Y.; Kunsunoki, M.; Harada, W.; Kakudo, M. J. Biochem. 1984, 95, 697-702. 22. Quiocho, F. A. Ann. Rev. Biochem. 1986, 55, 287-315. 23. Waldron, K. W.; Brett, C. T. Biochem. J. 1983, 213, 115-22. 24. Waldron, K. W.; Brett C. T. In Biochemistry of Plant Cell Walls; SEB Seminar Series 1985; 28, 79-97. 25. Ray, P. M. Biochim. Biophys. Acta 1980, 629, 431-44. 26. Hayashi, T.; Matsuda, K. J. Biol. Chem. 1981, 256, 11117-22. 27. Hayashi, T.; Matsuda, K. Plant and Cell Physiol. 1981, 22, 1571-84. 28. Jacob, S. R.; Northcote, D. H. J. Cell Sci. 1985 Suppl.2, 1-11. 29. Campbell, R. E.; Brett, C. T.; Hillman, J. R. Biochem. J. 1988, in press.



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POLYMERS

30. von Figura, Κ.; Hasilik, A. Ann. Rev. Biochem. 1986, 55, 167-93. 31. Pfeffer, S. R.; Rothmann, J. E. Ann. Rev. Biochem. 1987, 56, 829-52. 32. Northcote, D. H. Encyclopedia of Plant Physiology 1982, New Series 14A, 637-55. 33. Boffey, S. Α.; Northcote, D. H. Biochem. J. 1975, 150, 433-40. 34. Northcote, D. H. In The Synthesis, Assembly and Turnover of Cell Surface Components; Elsevier/North-Holland Biomedical Press, 1977; 4, 717-39. 35. Jahnen, W.; Hahlbrock, K. Planta 1988, 173, 453-8. 36. Rubery, P. H.; Northcote, D. H. Nature 1968, 219, 1230-34. 37. Haddon, L. E.; Northcote, D. H. J. Cell Sci. 1975, 17, 11-26. 38. Kuboi, T.; Yamada, Y. Biochim. Biophys. Acta 1978, 542, 181-90. 39. Fukuda, H.; Komamine, A. Planta 1982, 155, 423-30. 40. Bevan, M.; Northcote, D. H. Planta 1979, 147, 77-81. 41. Bevan, M.; Northcote, D. H. J. Cell Sci. 1979, 39, 339-53. 42. Jones, D. H.; Northcote, D. H. Eur. J. Biochem. 1981, 116, 117-25. 43. Bevan, M.; Northcote, D. H. Planta 1981, 152, 32-35. 44. Bevan, M.; Northcote, D. H. Planta 1981, 152, 24-31. 45. Poulton, J. E. In The Biochemistry of Plants: Secondary Plant Prod ucts; Academic Press: London, 1981; 7, 667-723. 46. Haddon, L.; Northcote, D. H. Planta 1976, 128, 255-62. 47. Butt, V. S.; Lamb, C. J. In The Biochemistry of Plants: Secondary Plant Products; Academic Press: London, 1981; 7, 627-65. 48. Amrhein, N.; Zenk, M. H. Naturwiss. 1970, 57, 312. 49. Hahlbrock, K.; Wellman, E. Biochim. Biophys. Acta 1973, 304, 702-6. 50. Hanson, K. R.; Havir, E. A. In The Biochemistry of Plants: Secondary Plant Products; Academic Press: London, 1981; 7, 577-625. 51. Grisebach, H. In The Biochemistry of Plant Products: Secondary Plant Products; Academic Press: London, 1981; 7, 457-78. 52. Alibert, G.; Ranjera, R.; Boudet, A. M. Physiol. Veg. 1977, 15, 279301. 53. Pryke, J. Α.; ap Rees, T. Planta 1976, 132, 279-89. 54. Pryke, J. Α.; ap Rees, T. Phytochem. 1977, 16, 557-60. 55. Ibrahim, R. K.; Grisebach, H. Arch. Biochem. Biophys. 1976, 176, 700-8. 56. Freudenberg, K. Science 1965, 148, 595-600. 57. Freudenberg, K. In Constitution and Biosynthesis of Lignin; Springer -Verlag: Berlin, 1968; 2, 45-122. 58. Yung, K.-H.; Northcote, D. H. Biochem. J. 1975, 151, 141-4. 59. Mader, M. Planta 1976, 131, 11-15. 60. Mader, M.; Nessel, Α.; Bopp, M. Z. Pflanzenphysiol. 1977, 82, 247-60. 61. Mader, M.; Amberg-Fisher, V. Pl. Physiol. 1982, 70, 1128-31. 62. Fry, S. C. Biochem. J. 1982, 204, 449-55. 63. Cooper, J. B.; Varner, J. E. Biochem. Biophys. Res. Commun. 1983, 112, 161-7. 64. Fry, S. C. Planta 1983, 157, 111-23. 65. Tanner, G. R.; Morrison, I. M. Phytochem. 1983, 22, 1433-39.



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66. Fry, S. C. Ann. Rev. Pl. Physiol. 1986, 37, 165-86. 67. Gould, J.; Northcote, D. H. In Bacterial Adhesion: Mechanisms and Physiological Significance; Plenum: New York, 1984; 89-110. 68. Cassab, G. I.; Varner, J. E. Nature 1986, 323, 110. 69. Lamport, D. T. A. In The Biochemistry of Plants: Carbohydrates; Aca demic Press: London, 1980; 3, 501-41. 70. Allen, A. K.; Dsai, Ν. N.; Neuberger, Α.; Creeth, J. M. Biochem. J. 1978, 171, 665-74. 71. Muray, R. Η. Α.; Northcote, D. H. Phytochem. 1978, 17, 623-9. 72. Fincher, G. B.; Stone, Β. Α.; Clarke, A. E. Ann. Rev. Pl. Physiol. 1983, 34, 47-70. 73. Cassab, G. I. Planta 1986, 168, 441-46. 74. Wienecke, K.; Glas, R.; Robinson, D. G. Planta 1982, 155, 58-63. 75. Blankenstein, P.; Lang, W. C.; Robinson, D. G. Planta 1986, 169, 238-44. 76. Sauer, Α.; Robinson, D. G. Planta 1985, 164, 287-94. 77. Owens, R. J.; Northcote, D. H. Biochem. J. 1981, 195, 661-7. 78. Hayashi, T.; Maclachlan, G. Biochem. J. 1984, 217, 791-803. 79. Hayashi, T.; Maclachlan, G. Phytochem. 1984, 23, 487-92. 80. Green, J. R.; Northcote, D. H. Biochem. J. 1978, 170, 599-608. 81. Green, J. R.; Northcote, D. H. Biochem. J. 1979, 178, 661-71. 82. Green, J. R.; Northcote, D. H. J. Cell Sci. 1979, 40, 235-44. 83. Ielpi, L.; Couso, R.; Dankert, R. FEBS Lett. 1981, 130, 253-56. 84. Ielpi, L.; Couso, R.; Dankert, R. Biochem. Biophys. Res. Comm. 1981, 102, 1400-8. 85. Couso, R. O.; Ielpi, L.; Garcia, R. C.; Dankert, R. Eur. J. Biochem. 1982, 123, 617-27. 86. Stumpf, P. K.; Shimakata, T. In Biosynthesis and Function of Plant Lipids Proc 6 University of California; Amer. Soc. Pl. Physiologists: Maryland, 1983; 1-27. 87. Nilsson-Ehle, P.; Garfinkel, A. S.; Schotz, M. C. Ann. Rev. Biochem. 1980, 49, 667-92. RECEIVED May 19, 1989


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