Stress Metabolites of White Potatoes - American Chemical Society

17 Stress Metabolites of White Potatoes GARNETT E. WOOD

Downloaded by CORNELL UNIV on May 24, 2017 | http://pubs.acs.org Publication Date: June 1, 1976 | doi: 10.1021/ba-1976-0149.ch017

Division of Chemistry and Physics, Bureau of Foods, Food and Drug Administration, U.S. Department of Health, Education, and Welfare, Washington, D.C. 20204 Many compounds are produced in white potatoes as a result of physiological stress imposed on the tissues. Stress conditions in a potato may result from exposure to light, injury, certain microorganisms, and extreme temperatures. The imposed stress may alter normal metabolic pathways in the potato resulting in the synthesis of abnormal amounts of a particular compound or may cause different metabolic pathways to be utilized thus giving rise to new or unusual compounds. The stress phenomenon results in the production of certain compounds including chlorogenic acid, scopolin, solanine, and chaconine in levels greater than that found in the normal tissue and in the production of other compounds like rishitin, phytuberin, lubimin, alpha-solamarine, and beta-solamarine which are not found in nonstressed tissue. The chemistry of these metabolites is reviewed, and the potential toxicological significance of the presence of these compounds in potatoes is discussed.

White potatoes (Solanum tuberosum) are widely used in many parts of the world as a staple food for man. Potatoes are susceptible to attack by various microorganisms and insects while in the field and during storage; they may also be subjected to mechanical damage during the harvesting operation. The imposition of any of these conditions on healthy potatoes will upset some normal physiological sequences thereby causing "stress" on the metabolic system. Stress can also be induced by certain chemical toxicants as well as by variations in temperature and environ mental factors. Stressed potatoes may be found to contain increased amounts of certain compounds that are normal constituents of the tissue or certain compounds that are not normally found in the tissue. In the latter case the pathways for the synthesis of these compounds must exist 369

Rodricks; Mycotoxins and Other Fungal Related Food Problems Advances in Chemistry; American Chemical Society: Washington, DC, 1976.

370

MYCOTOXINS

i n the tissue, y e t t h e y m a y n o t b e a c t i v a t e d or u t i l i z e d unless the u s u a l m e t a b o l i c p a t h w a y s b e c o m e a l t e r e d o r d a m a g e d as a result of stress c o n d i t i o n s . I n p l a n t s stress m e t a b o l i t e s are s y n t h e s i z e d b y m o d i f y i n g e i t h e r the shikimic acid, acetate-malonate, or acetate-mevalonate

pathways.

U n u s u a l c o m p o u n d s p r o d u c e d b y p l a n t s i n response to v a r i o u s exoge nous s t i m u l i are g e n e r a l l y r e f e r r e d to as p h y t o a l e x i n s . T h i s t e r m w a s i n t r o d u c e d b y M i i l l e r a n d B o r g e r ( I ) to define a c h e m i c a l c o m p o u n d p r o d u c e d o n l y w h e n the l i v i n g cells of the host are i n v a d e d b y a p a r a s i t e a n d u n d e r g o necrobiosis.

T h a t d e f i n i t i o n w a s later m o d i f i e d b y

Miiller

( 2 ) as a result of f u r t h e r studies a n d w a s restated as " a n t i b i o t i c s w h i c h


are p r o d u c e d as a result of the i n t e r a c t i o n of t w o m e t a b o l i c systems, host a n d p a r a s i t e , a n d w h i c h i n h i b i t the g r o w t h of m i c r o o r g a n i s m s p a t h o g e n i c to p l a n t s . " A d e t a i l e d d e s c r i p t i o n of t h e properties of p h y t o a l e x i n s a n d t h e i r r o l e i n h o s t - p a r a s i t e interactions w a s presented i n reviews b y C r u i c k shank (3)

a n d C r u i c k s h a n k a n d P e r r i n (4).

A m o r e recent r e v i e w o n

p h y t o a l e x i n s w a s w r i t t e n b y K u c ( 5 ) b a s e d o n the c o n c e p t t h a t " t h e t e r m p h y t o a l e x i n s s h o u l d serve as a n u m b r e l l a u n d e r w h i c h c h e m i c a l

com

p o u n d s c o n t r i b u t i n g to disease resistance c a n b e classified w h e t h e r t h e y are f o r m e d i n response to i n j u r y , p h y s i o l o g i c a l s t i m u l i , a n d the presence of i n f e c t i o u s agents or are the p r o d u c t s of s u c h agents." A s i m i l a r d e f i n i t i o n w a s u s e d b y K i r a ' l y ( 6 ) w h o defined p h y t o a l e x i n s as substances p r o d u c e d b y p l a n t s after i n f e c t i o n a n d adverse treatments a n d r e s p o n s i b l e f o r resistance to i n f e c t i n g agents. P r i o r to 1972 interest i n c o m p o u n d s p r o d u c e d i n plants as a r e s u l t of stress c o n d i t i o n s w a s c e n t e r e d a r o u n d the d e v e l o p m e n t of a n u n d e r s t a n d i n g of the b i o c h e m i c a l basis of disease resistance i n plants. E x c e l l e n t r e v i e w s o n p h y t o a l e x i n s a n d c o m p o u n d s a c c u m u l a t i n g i n plants after i n f e c tion have been presented b y K u c (5, 7 ) .

C u r r e n t l y , particular emphasis

is o n stress m e t a b o l i t e s t h a t a c c u m u l a t e i n the tubers of w h i t e potatoes b e c a u s e of a r e p o r t b y R e n w i c k ( 8 ) w h i c h i m p l i e d that c e r t a i n potatoes c o n t a i n e d a specific b u t u n i d e n t i f i e d c o m p o u n d t h a t caused b i r t h defects i n humans. The compound

( c o m p o u n d s ) w a s b e l i e v e d to be

produced

as a r e s u l t of exposure of the p o t a t o to stress c o n d i t i o n s , p a r t i c u l a r l y e x p o sure to the m o l d Phytophthora

infestans,

t h e causative agent of l a t e b l i g h t .

T h i s h y p o t h e s i s w a s s u p p o r t e d b y e p i d e m i o l o g i c a l d a t a that s h o w e d c o r r e l a t i o n s b e t w e e n i n c i d e n c e of b i r t h defects, potato b l i g h t , a n d

potato

c o n s u m p t i o n b y g e o g r a p h i c r e g i o n , y e a r , a n d i n c o m e group. E x p e r i m e n t a l e v i d e n c e s u p p o r t i n g the presence of a teratogenic agent i n b l i g h t e d p o t a toes w a s later p r e s e n t e d b y P o s w i l l o et a l . ( 9 ) .

T h i s evidence w a s b a s e d

o n observations m a d e w h e n c o t t o n - e a r e d marmosets w e r e f e d a d i e t w h i c h i n c l u d e d sprouted, unpeeled, irradiated, boiled, freeze-dried potatoes.

blighted

F o u r of e l e v e n fetuses f r o m six females t h a t h a d c o n s u m e d the

d i e t f o r a p e r i o d of t i m e s h o w e d a b n o r m a l c r a n i a l defects; n o


defects

17.

WOOD

Stress

371

Metabolites

w e r e o b s e r v e d i n fetuses f r o m females i n a c o n t r o l g r o u p that d i d n o t c o n s u m e potatoes i n t h e i r diet. I n f u r t h e r experiments i n w h i c h p r e g n a n t marmosets w e r e g i v e n a m i x t u r e of potatoes that w e r e b l i g h t e d a n d other w i s e d a m a g e d n o gross a b n o r m a l i t i e s w e r e o b s e r v e d , b u t b e h a v i o r i a l d e fects w e r e n o t e d ( 1 0 ) .

S i n c e t h e n , other investigators h a v e c i t e d d a t a ,

e p i d e m i o l o g i c a l a n d e x p e r i m e n t a l , w h i c h s h o w inconsistencies i n the r e l a t i o n s h i p b e t w e e n the c o n s u m p t i o n of b l i g h t e d potatoes a n d b i r t h defects (II,

12,13,14,15). T h e p u r p o s e of this p a p e r is to r e v e a l those c o m p o u n d s that are c o n

s i d e r e d stress metabolites i n w h i t e potatoes a n d to r e v i e w t h e i r c h e m i s t r y


a n d i n f o r m a t i o n t h a t is k n o w n a b o u t t h e i r t o x i c i t y . A r e p o r t c o n c e r n i n g metabolites a c c u m u l a t i n g i n p o t a t o tubers f o l l o w i n g i n f e c t i o n a n d stress r e c e n t l y a p p e a r e d i n the l i t e r a t u r e

(16).

Normal Constituents Whose Concentrations Increase Because of Stress T h e s t r u c t u r e a n d c h e m i c a l c o m p o s i t i o n of the p o t a t o t u b e r w a s r e v i e w e d b y S c h w i m m e r a n d B u r r (17).

T h e c h e m i c a l c o m p o s i t i o n of the

p o t a t o differs w i t h t h e v a r i e t y , age, c o n d i t i o n of g r o w t h , a n d e v e n i n d i v i d u a l differences,

b u t these v a r i a b l e s f a l l w i t h i n w e l l - d e f i n e d l i m i t s

(18). Glycoalkaloids.

A l t h o u g h t h e p o t a t o contains m a n y types of

com

p o u n d s , some of w h i c h h a v e i n t r i n s i c t o x i c p r o p e r t i e s , o n l y solanine or the g l y c o a l k a l o i d s are h a z a r d o u s to m a n (19).

T h e a l k a l o i d s t h a t are n o r m a l l y

f o u n d i n the w h i t e p o t a t o are d e r i v a t i v e s of the s t e r o i d base s o l a n i d i n e ( F i g u r e 1 ) . T h i s base ( a g l y c o n e ) contains a n a l c o h o l h y d r o x y l g r o u p , a r e d u c i b l e d o u b l e b o n d a n d a t e r t i a r y n i t r o g e n t h a t does n o t b e a r a m e t h y l g r o u p a n d has f o u r C - m e t h y l groups a n d the c o m p o s i t i o n

C27H43ON

(20).

T h e a l k a l o i d s i n potatoes are r e f e r r e d to as g l y c o a l k a l o i d s b e c a u s e t h e y

L-Rho Figure 1.

Major glycoalkaloids

in white potatoes


372

MYCOTOXINS

exist as glycosides o r acetals r e s u l t i n g f r o m a c o m b i n a t i o n of a s t e r o i d base w i t h v a r i o u s sugars. T h e t w o m a j o r g l y c o a l k a l o i d s i n potatoes

are

α - s o l a n i n e a n d α - c h a c o n i n e ; b o t h c o n t a i n t h e s o l a n i d i n e b a s e b u t differ i n their carbohydrate components.

S o l a n i n e contains one m o l e of

glucose,

one m o l e of galactose, a n d o n e m o l e of r h a m n o s e ; c h a c o n i n e contains one m o l e of glucose a n d t w o moles of r h a m n o s e . α - S o l a n i n e a n d α - c h a c o n i n e a c c o u n t for 9 5 %

of t h e t o t a l g l y c o a l k a l o i d s i n potatoes

(21).

Other

g l y c o a l k a l o i d s f o u n d i n s m a l l e r amounts i n c l u d e β - a n d γ-solanine a n d β- a n d γ - c h a c o n i n e ( 2 2 ) ; these are p r o d u c t s r e s u l t i n g f r o m t h e p a r t i a l h y d r o l y s i s of α - s o l a n i n e a n d α - c h a c o n i n e . T h e presence of glycosidases i n


p o t a t o sprouts t h a t h y d r o l y z e «-solanine a n d α - c h a c o n i n e w a s strated b y G u s e v a a n d P a s e s h n i c h e n k o (21).

demon

M o s t studies h a v e

been

c o n d u c t e d o n α - s o l a n i n e a n d α - c h a c o n i n e because t h e y are u s u a l l y t h e major components

of the p o t a t o a l k a l o i d s . I n m a n y reports t h e t e r m

s o l a n i n e is u s e d to refer to a m i x t u r e of t h e t w o c o m p o u n d s since t h e y are n o t easily separable. T h e s e c o m p o u n d s h a v e b e e n r e p o r t e d to exist i n a r a t i o of one solanine to t w o c h a c o n i n e i n several varieties of potatoes ( 2 3 , 24).

S o m e reports i n the l i t e r a t u r e c o n t a i n d a t a o n t o t a l g l y c o a l k a

loids without differentiating between solanine a n d chaconine. T h e a m o u n t of t o t a l g l y c o a l k a l o i d s i n n o r m a l h e a l t h y potatoes

can

b e affected b y s u c h factors as l o c a t i o n , c o n d i t i o n s of g r o w t h , v a r i e t y , a n d storage c o n d i t i o n s . I n a d e t a i l e d s t u d y b y W o l f a n d D u g g a r ( 2 5 ) i n v o l v i n g 32 varieties of potatoes g r o w n i n W i s c o n s i n the t o t a l g l y c o a l k a l o i d c o n t e n t i n h e a l t h y potatoes r a n g e d f r o m 1.8-13 m g % w i t h 7 5 % of t h e varieties b e t w e e n 3.2 a n d 9.4 m g % . a n d W e b b (26)

five

I n a more recent study b y Sinden

c o m m e r c i a l varieties of potatoes g r o w n at 3 9 l o c a

tions t h r o u g h o u t the U n i t e d States w e r e a n a l y z e d for t o t a l g l y c o a l k a l o i d s content. T h e average g l y c o a l k a l o i d c o n t e n t of the five varieties tested i n 1970 w a s 7.2 m g / 1 0 0 g. I n 1971 the average content for three c o m m e r c i a l varieties w a s 9.0 m g / 1 0 0 g for a l l l o c a t i o n s .

E x c e s s i v e (20 m g / 1 0 0

g)

g l y c o a l k a l o i d contents for samples of the five varieties f r o m c e r t a i n l o c a tions w e r e a t t r i b u t e d to u n u s u a l e n v i r o n m e n t a l c o n d i t i o n s or postharvest h a n d l i n g p r o c e d u r e s at the p a r t i c u l a r l o c a t i o n . T h e s o l a n i n e c o n t e n t of potatoes has b e e n o b s e r v e d to increase as a r e s u l t of exposure to l i g h t of v a r i o u s intensities (27, 28, 29) a n d v a r i o u s temperatures (30). b y S a l u n k h e et a l . (30)

I n studies

p o t a t o slices w e r e d i v i d e d i n t o t w o g r o u p s :

w a s stored i n the d a r k , a n d t h e other e x p o s e d to

fluorescent

light.

g r o u p w a s s u b j e c t e d to different storage t e m p e r a t u r e s r a n g i n g f r o m

one Each 0°-

24 ° C . A f t e r 48 h r at 24 ° C i n t h e d a r k the solanine l e v e l h a d i n c r e a s e d to s e v e n times as m u c h as i n the o r i g i n a l c o n t r o l s a m p l e s ; after 48 h r as 24 ° C i n the l i g h t the s o l a n i n e l e v e l w a s three t o f o u r times greater t h a n t h a t o b s e r v e d i n the d a r k . T h e authors c o n c l u d e d t h a t this p h e n o m e n o n m a y b e a f o r m of p h y s i o l o g i c a l defense m e c h a n i s m i n tubers or slices


17.

WOOD

Stress

373

Metabolites

w h e n e x p o s e d to a stress s u c h as h i g h l i g h t i n t e n s i t y t h a t m i g h t o c c u r i n g r o c e r y stores or w o u n d i n g as i n the case of slices o r strips p r e p a r e d for c h i p s o r f r e n c h fries. I n a n e a r l i e r s t u d y b y K u c (31)

it was observed

that t h e levels of solanine a n d c h a c o n i n e increase s i g n i f i c a n t l y i n potato slices t h a t w e r e stored i n the d a r k at r o o m t e m p e r a t u r e for three days. S o l a n i d i n e , the a g l y c o n e of s o l a n i n e a n d c h a c o n i n e , has b e e n n o t e d to a c c u m u l a t e i n c e r t a i n varieties of potatoes.

Z i t n a k (32)

found that

u n d e r c o n d i t i o n s of intense solar r a d i a t i o n a l t e r n a t e d w i t h exposure n e a r f r e e z i n g temperatures, w h i c h f r e q u e n t l y o c c u r d u r i n g the

to

potato

harvest i n n o r t h e r n areas, s o l a n i d i n e is r a p i d l y p r o d u c e d i n excess of


amounts t h a t c o u l d b e b o u n d as solanine. T h e l e v e l of solanine a n d c h a c o n i n e i n potatoes is k n o w n to increase as a result of w o u n d i n g ( 3 3 ) .

L o c c i a n d K u c (34)

n o t e d a n increase i n

these a l k a l o i d s i n a g e d n o n i n o c u l a t e d s l i c e d tissue. T h e y c o n c l u d e d t h a t the a l k a l o i d s a c c u m u l a t e d i n response to p h y s i o l o g i c a l stress w h i c h w a s i n d u c e d b y m e c h a n i c a l i n j u r y . I t has b e e n d e m o n s t r a t e d t h a t a l k a l o i d s are l a r g e l y r e s t r i c t e d to the p e e l of w h o l e potatoes, b u t i n j u r y c a u s e d b y s l i c i n g results i n i n c r e a s e d synthesis a n d a c c u m u l a t i o n i n p e e l e d potatoes O t h e r investigators h a v e also o b s e r v e d a n a c c u m u l a t i o n of g l y c o

(24).

a l k a l o i d s at t h e surface of c u t tissue ( 3 5 , 36, 37).

S h i h et a l . (37)

noted

h o w e v e r t h a t the a c c u m u l a t i o n is s u p p r e s s e d s i g n i f i c a n t l y i f the c u t tissue is i n o c u l a t e d w i t h Phytophthora

T h i s suggests t h a t the b i o

infestans.

s y n t h e t i c p a t h w a y f o r g l y c o a l k a l o i d p r o d u c t i o n c a n b e f u r t h e r a l t e r e d as a result of a d d i t i o n a l stress i m p o s e d b y i n f e c t i o n w i t h m i c r o o r g a n i s m s . M a n y cases of h u m a n p o i s o n i n g h a v e b e e n a t t r i b u t e d to the c o n s u m p t i o n of potatoes ( 3 8 ) .

I n some of the r e p o r t e d cases, analyses of the sus

p e c t e d potatoes for t o t a l g l y c o a l k a l o i d s w e r e m a d e , a n d i t w a s f o u n d t h a t a l l of the potatoes i n v o l v e d h a d a n a b n o r m a l l y h i g h s o l a n i n e content.

A

g l y c o a l k a l o i d content of 20 m g / 1 0 0 g of p o t a t o tissue is c o n s i d e r e d toxic for h u m a n s ( 3 9 ) .

I n experiments w i t h humans it was f o u n d that an oral

dose of 200 m g of solanine c a n cause drowsiness a n d l a b o r e d b r e a t h i n g ; h i g h e r doses c a u s e d v o m i t i n g a n d d i a r r h e a (40).

A n extensive p h a r m a

c o l o g i c a l s t u d y of s o l a n i n e w a s c a r r i e d o u t b y N i s h i e et a l . (41).

Solanine

w a s f o u n d to b e t o x i c to c h i c k e m b r y o s , m i c e , rats, a n d r a b b i t s w h e n a d ministered parenterally. T h e L D

5 0

values i n chick embryos

injection) and i n mice and rabbits ( i p )

(yolk

sac

w e r e 18.8, 42, a n d 20 m g / k g ,

r e s p e c t i v e l y . O r a l a d m i n i s t r a t i o n of 1 g / k g p r o d u c e d n o toxic effects i n m i c e . S o l a n i d i n e , the a g l y c o n e , w a s less t o x i c t h a n s o l a n i n e ; i t w a s n o n t o x i c to m i c e at 500 m g / k g I P . T h e s e investigators c o n c l u d e d f r o m t h e i r findings

t h a t the r e l a t i v e l y r a r e o c c u r r e n c e

of solanine p o i s o n i n g

from

potatoes a n d the l o w o r a l t o x i c i t y of s o l a n i n e f o r l a b o r a t o r y a n i m a l s m a y b e e x p l a i n e d o n the basis of p o o r a b s o r p t i o n f r o m t h e g a s t r o i n t e s t i n a l tract, r a p i d u r i n a r y a n d f e c a l e x c r e t i o n of m e t a b o l i t e s , a n d g a s t r o i n t e s t i n a l


374

MYCOTOXINS

H< HO

HOO

Stress Metabolites of White Potatoes - American Chemical Society

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