Interactions between Phytophthora Infestans and Potato Host

4 Interactions between Phytophthora Infestans and Potato Host

Downloaded by CORNELL UNIV on August 23, 2016 | http://pubs.acs.org Publication Date: June 1, 1977 | doi: 10.1021/bk-1977-0062.ch004

DONALD D. BILLS Eastern Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, Philadelphia, PA 19118

The white potato (Solanum tuberosum) was unknown outside of South America until the sixteenth century, but by the nineteenth century, it was widely cultivated in the British Isles, Europe, Russia, and the United States. Ireland, in particular, shifted its agricultural emphasis from cereal grains to the more productive potato with such success that the population of Ireland increased considerably to about 7 million by 1844. In 1845, climatic conditions and widespread growth of the potato in Ireland permitted catastrophic field infection by Phytophthora infestans and resulted in the loss of nearly the entire potato crop in that year and the subsequent year. The results for Ireland were devastating; over one million people died of starvation or diseases associated with malnutrition, and over one million more emigrated. P. infestans, the pathogen responsible for potato late blight, remains the most significant fungal parasite of the potato. The Nature of Late Blight The symptoms of late blight on the potato plant are visible first as dark brown patches on the leaflets, usually near the margin. On the leaflets of varieties that are incompatible with the infecting race of P. infestans, the necrosis is restricted to small spots or flecks that do not enlarge. In a susceptible interaction, the necrotic areas expand, and white mold growth is usually visible along their edges on the underside of the leaflet. If weather conditions remain sufficiently damp, the infection can spread and destroy the entire haulm in a period of several weeks. During the course of progressive infection, spores are spread to other plants by wind, rain, or insects and transferred to the soil and the tubers of infected plants by rain. The means by which late blight is perpetuated are shown in Fig. 1. In the vicinity of potato fields, elimination of cull piles containing blighted tubers is a well-accepted practice for 47 American Chemical Society Library 1155 16th St.N.W. Hedin; Host Plant to Pests Washington, D.Resistance C. 20036 ACS Symposium Series; American Chemical Society: Washington, DC, 1977.


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c o n t r o l l i n g the spread of i n f e c t i o n from t h i s source, and the s e l e c t i o n of seed tubers as f r e e from i n f e c t i o n as p o s s i b l e i s recognized as a n e c e s s i t y . One b l i g h t e d seed tuber i n 100,000 provides an adequate i n i t i a l inoculum f o r a major epidemic (1). C o n t r o l of the spread of i n f e c t i o n between potato p l a n t s i s dependent upon the use of f u n g i c i d e s such as the e t h y l e n e b i s d i t h i o carbamates and the p l a n t i n g of potato v a r i e t i e s that have some degree of r e s i s t a n c e . In the United States, the use of f u n g i c i d e s to prevent the spread of l a t e b l i g h t g e n e r a l l y i s p r a c t i c e d i n a l l areas except the western s t a t e s where the summer climate i s u s u a l l y dry and unconducive to the development of l a t e b l i g h t . Under current management p r a c t i c e s i n the United States, l a t e b l i g h t decreases the y i e l d of potatoes at harvest by about 4%. Further l o s s e s are encountered i n storage when tubers with minor b l i g h t e d areas become mixed i n a d v e r t e n t l y w i t h sound tubers. P^. i n f e s t a n s does not g e n e r a l l y spread to healthy tubers during storage, but the l o c i of i n f e c t i o n provide footholds f o r secondary b a c t e r i a l i n f e c t i o n s that spread to other tubers and cause s i g n i f i cant l o s s e s (2). Potato Resistance

to Fungal I n f e c t i o n

The potato i s immune to p a r a s i t i z a t i o n by the vast m a j o r i t y of f u n g i ; there are, i n c l u d i n g _P. i n f e s t a n s , only s i x or seven fungal p a r a s i t e s of the p l a n t and tuber that are economically s i g n i f i c a n t (2). The term immunity i s used to denote complete and apparently permanent p r o t e c t i o n against a given p a r a s i t e , whereas r e s i s t a n c e denotes e i t h e r incomplete or impermanent p r o t e c t i o n . P a r a l l e l s have been drawn between immunity and r e s i s t a n c e (1_, 3), but Robinson (_1) suggests that immunity i s outside of the conceptual bounds of p a r a s i t i s m . Perhaps the major d i f f i c u l t y i n c o n c e p t u a l i z i n g immunity i s that no one yet has formulated a research approach that might lead to a d e s c r i p t i o n of the circumstances r e s p o n s i b l e f o r the immune r e l a t i o n s h i p of p l a n t s to f u n g i . Resistance, on the other hand, provides chemically and p h y s i c a l l y observable and measurable phenomena as a b a s i s f o r research. Resistance to fungal p a r a s i t e s commonly i s d i v i d e d i n t o two general c a t e g o r i e s , h o r i z o n t a l r e s i s t a n c e and v e r t i c a l r e s i s t a n c e . H o r i z o n t a l r e s i s t a n c e i s s a i d to provide a constant l e v e l (high, moderate, low, or n e a r l y zero) of i n f e c t a b i l i t y w i t h a l l e x i s t i n g and p o t e n t i a l races of a given fungal s p e c i e s . From the constant l e v e l of i n f e c t a b i l i t y , the term and concept of h o r i z o n t a l r e s i s t ance was formulated by van der Plank (4). I t i s b e l i e v e d that h o r i z o n t a l r e s i s t a n c e u s u a l l y has a polygenic o r i g i n i n the host and that mechanisms r e s p o n s i b l e f o r h o r i z o n t a l r e s i s t a n c e are l i k e l y to be numerous and complex. I f t h i s were not the usual case, minor genetic changes i n a fungal p a r a s i t e would be more l i k e l y to r e s u l t i n new races capable of p a r a s i t i z i n g the host at higher l e v e l s .

Hedin; Host Plant Resistance to Pests ACS Symposium Series; American Chemical Society: Washington, DC, 1977.


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Phytophthora Infestans and

Potato

Host

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H o r i z o n t a l r e s i s t a n c e can be viewed s p e c u l a t i v e l y as a b a r r i e r of p h y s i c a l or chemical defenses which slow fungal i n v a s i o n . U n a v a i l a b i l i t y i n the host of adequate e s s e n t i a l n u t r i e n t s required f o r fungal growth would c o n s t i t u t e a passive form of h o r i z o n t a l r e s i s t a n c e . The concept of h o r i z o n t a l r e s i s t a n c e can a l s o be extended to chemicals a p p l i e d e x t e r n a l l y . The e f f e c t i v e n e s s of new f u n g i c i d e s i s o f t e n temporary because the f u n g i produce new races unaffected by them. Other f u n g i c i d e s , such as Bordeaux Mixture, appear to have " h o r i z o n t a l p r o p e r t i e s " and maintain t h e i r e f f e c t i v e n e s s permanently, i n d i c a t i n g that the f u n g i are unable to produce new races able to t o l e r a t e them. The i n a b i l i t y of f u n g i to circumvent the t o x i c i t y of the " h o r i z o n t a l " d i t h i o carbamate f u n g i c i d e s , which i n h i b i t twenty or more enzymes (5), i s e a s i l y understood. The presence of a " n a t u r a l h o r i z o n t a l f u n g i c i d e " i n host t i s s u e would confer some degree of r e s i s t a n c e , and there i s evidence, c i t e d l a t e r , that the potato tuber contains indigenous compounds with f u n g i t o x i c p r o p e r t i e s . While potato v a r i e t i e s can e x h i b i t v a r y i n g degrees of h o r i z o n t a l r e s i s t a n c e to P^. i n f e s t a n s , most commercial v a r i e t i e s have (and most breeding programs are aimed at producing) v e r t i c a l r e s i s t a n c e ( 1 ) . The term v e r t i c a l r e s i s t a n c e i s derived from the observation that i n some h o s t - p a r a s i t e i n t e r a c t i o n s i n f e c t i o n of a given host v a r i e t y by d i f f e r e n t fungal races can occur at e i t h e r a high l e v e l ( s u s c e p t i b l e or compatible i n t e r a c t i o n ) or a very low l e v e l ( r e s i s t a n t , incompatible, or h y p e r s e n s i t i v e i n t e r a c t i o n ) ( 4 ) . The terms compatible and incompatible are used i n the remainder of t h i s paper. V e r t i c a l r e s i s t a n c e i s o f t e n r e f e r r e d to as a gene-for-gene r e l a t i o n s h i p between host and fungal p a r a s i t e ( 1 ). Obviously, i t i s not the genes but the chemical and p h y s i c a l c h a r a c t e r i s t i c s whose i n h e r i t a n c e i s g e n e t i c a l l y c o n t r o l l e d that e i t h e r match or do not match each other. Albersheim and AndersonProuty ( 6 ) e x t e n s i v e l y reviewed the evidence f o r the existence of g e n e t i c a l l y c o n t r o l l e d r e c o g n i t i o n mechanisms that r e s u l t i n an incompatible response between fungal p a r a s i t e and p l a n t h o s t . A formal c l a s s i f i c a t i o n scheme has been e s t a b l i s h e d to designate the genetic r e l a t i o n s h i p between potato v a r i e t i e s and ]?. i n f e s t a n s races i n terms of c o m p a t i b i l i t y and i n c o m p a t i b i l i t y ( 7 ) . In t h i s widely accepted scheme, potato v a r i e t i e s are described as posses s i n g v e r t i c a l r e s i s t a n c e genes designated as R i , R 2 , R 3 , e t c . A s i n g l e potato v a r i e t y may possess zero, one, or m u l t i p l e r e s i s t a n c e genes. Ρ_. i n f e s t a n s races are described as possessing pathogenici ty genes designated as v^, V 2 , V 3 , e t c . (or as race 1 , race 2 , race 3 , e t c . ) , and a s i n g l e race may possess zero, one, or m u l t i p l e p a t h o g e n i c i t y genes. A potato v a r i e t y having the s i n g l e r e s i s t a n c e gene R 2 i n t e r a c t s i n a compatible manner w i t h P^. i n f e s t a n s races with the V 2 gene and i n an incompatible manner with a l l other races. Such a scheme has great u t i l i t y as a c l a s s i f i c a t i o n system, but i t s e m p i r i c a l nature must be kept i n mind. The designations used have no r e a l meaning apart from the observed i n t e r a c t i o n s between host and p a r a s i t e .


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Not a l l i n v e s t i g a t o r s b e l i e v e that r e s i s t a n c e can be n e a t l y categorized as e i t h e r h o r i z o n t a l or v e r t i c a l . A l s o , both types of r e s i s t a n c e may e x i s t simultaneously i n a s i n g l e c u l t i v a r , although strong v e r t i c a l r e s i s t a n c e u s u a l l y tends to mask h o r i zontal resistance.


Native P r o p e r t i e s Related to Resistance The potato p l a n t and tuber have n a t i v e p h y s i c a l and chemical p r o p e r t i e s r e l a t e d to r e s i s t a n c e . The epidermis of the f o l i a r p o r t i o n of the p l a n t and the s k i n of the tuber present p h y s i c a l b a r r i e r s to fungal and b a c t e r i a l i n f e c t i o n . A moist environment i s r e q u i r e d to permit spore germination and f u n g a l i n v a s i o n across these primary defenses. The stomata of the l e a f l e t s and the l e n t i c e l s of the tuber represent weak p o i n t s i n the primary defenses, but wounding provides a more immediate f o o t h o l d f o r fungal i n v a s i o n . As described by Kuc and C u r r i e r (8), a number of indigenous compounds which have some degree of f u n g i t o x i c i t y are found a t higher l e v e l s i n the outer few m i l l i m e t e r s of the tuber. These compounds are c h l o r o g e n i c a c i d , c a f f e i c a c i d , g l y c o a l k a l o i d s , and s c o p o l i n . The l e v e l s of c h l o r o g e n i c a c i d (9), c a f f e i c a c i d (10), and g l y c o a l k a l o i d s (11, 12) i n c r e a s e i n mechanically wounded tuber t i s s u e , thus adding, perhaps, some degree of p r o t e c t i o n i n an otherwise v u l n e r a b l e s i t u a t i o n . Rapid s u b e r i z a t i o n followed by formation of a wound periderm i n as l i t t l e as 24 hr (2) i s probably more important as a defense. Scopolin and i t s aglycone s c o p o l e t i n are normally present i n potato tubers. The s c o p o l e t i n content of tubers v a r i e s with the p h y s i o l o g i c a l s t a t e , being highest i n newly-harvested, dormant tubers (13). Mechanical d i s r u p t i o n of tuber t i s s u e does not i n c r e a s e the c o n c e n t r a t i o n of s c o p o l i n , but i n f e c t i o n by P^. i n f e s t a n s , other f u n g i , b a c t e r i a , and v i r u s e s causes s i g n i f i c a n t increases (14, 15). Compounds Produced i n I n f e c t e d Potato T i s s u e The incompatible i n t e r a c t i o n of P^. i n f e s t a n s with potato t i s s u e leads to the production of a number of compounds that are not n a t i v e to the host. Studies have been c a r r i e d out predomin a n t l y with tuber t i s s u e d i s r u p t e d by s l i c i n g p r i o r to i n o c u l a t i o n and care must be e x e r c i s e d i n attempting to e x t r a p o l a t e such f i n d i n g s to events that may t r a n s p i r e i n i n t a c t f o l i a r t i s s u e during f i e l d i n f e c t i o n . Zacharius e t a l . (16) have shown that tuber t i s s u e may not even provide a corresponding compatible or incompatible response when compared to the l e a f l e t s of the same potato v a r i e t y . The terpenoid s t r u c t u r e s that have been i s o l a t e d and charact e r i z e d as products of an incompatible i n t e r a c t i o n between _P. i n f e s t a n s and potato tuber t i s s u e are shown i n F i g . 2. Tomiyama



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Host

Figure 1. Cycle of Phytophthora infestans in fection of Solanum tuberosum. Points at which the spread of infection may be disrupted effec tively are indicated at 1,2, and 3.

KATAHDINONE

LUBIMIN

DEHYDROKATAHDINONE

ISOLUBIMIN

OXYLUBIMIN

RISHITIN

Ο RISHITINOL

PHYTUBERIN

Figure 2. Compounds produced by the potato tuber host in response to infection. Most of these compounds have dem onstrated fungitoxic properties and are often referred to as phytoalexins.



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et a l . i s o l a t e d r i s h i t i n from i n f e c t e d R i s h i r i v a r i e t y potatoes (17), and K a t s u i et a l . c h a r a c t e r i z e d t h i s compound (18). K a t s u i ejt a l . (19, 20) i s o l a t e d and c h a r a c t e r i z e d r i s h i t i n o l . Varns et_ a l . (21) i s o l a t e d phytuberin, and Hughes and Coxon (22) e s t a b l i s h e d i t s s t r u c t u r e . M e t l i t s k i i et a l . (23) f i r s t i s o l a t e d l u b i m i n from a Soviet potato v a r i e t y , Lyubimets, and S t o e s s l et a l . (24) and K a t s u i et a l . (25) determined i t s s t r u c t u r e . K a t s u i et a l . (25) i s o l a t e d and i d e n t i f i e d oxylubimin; Kalan and Osman (26), i s o l u b i m i n . I n v e s t i g a t o r s i n England and i n the U.S. Department of A g r i c u l t u r e (27) simultaneously i s o l a t e d and i d e n t i f i e d katahdinone and dehydrokatahdinone. The t r i v i a l name, katahdinone, was d e r i v e d from the Katahdin potato v a r i e t y from which the compound was i s o l a t e d i n the United S t a t e s . The use of potato tuber s l i c e s i n the above s t u d i e s i s advantageous i n that many potato c e l l s are i n f e c t e d , i n o c u l a t e d s l i c e s can be incubated under c o n t r o l l e d c o n d i t i o n s , and the production of terpenoids i s high per u n i t mass of potato t i s s u e . The production of compounds i n the incompatible i n t e r a c t i o n i n i n t a c t f o l i a r t i s s u e i s more d i f f i c u l t to study because the i n f e c t i o n i s r e s t r i c t e d to very small areas. M e t l i t s k i i et a l . reported lubimin production i n potato l e a f l e t s i n o c u l a t e d with ]?. i n f e s t a n s (28). T h i s suggests, a t l e a s t , that terpenoid production may not be p e c u l i a r to tuber t i s s u e . While the above terpenoids have been i s o l a t e d from incomp a t i b l e i n t e r a c t i o n s between !P. i n f es tans and potato tuber t i s s u e , t h i s i s not the e x c l u s i v e mechanism f o r t h e i r p r o d u c t i o n . Zacharius et a l . (29) reported that r i s h i t i n was produced i n both a compatible i n t e r a c t i o n and an incompatible i n t e r a c t i o n a t a s i m i l a r r a t e during the f i r s t and second days f o l l o w i n g i n o c u l a t i o n . Other r e p o r t s document the production of r i s h i t i n , phytuberin, and lubimin i n potato tuber t i s s u e invaded by E r w i n i a carotovora v a r . a t r o s e p t i c a (30, 31, 32). The formation of terpenoids i n potato tuber t i s s u e c h e m i c a l l y t r e a t e d with NaF was reported by M e t l i t s k i i et a l . (33), but t h i s experiment could not be d u p l i c a t e d by Zacharius et a l . (34). In a d d i t i o n to the production of terpenoids, d e t e c t a b l e changes i n the s o l u b l e p r o t e i n patterns of potato t i s s u e i n t e r a c t i n g incompatibly with ]?. i n f e s t a n s have been r e p o r t e d . In i n f e c t e d tuber t i s s u e , Tomiyama and Stahman found an i n c r e a s e d number of e l e c t r o p h o r e t i c a l l y separable p r o t e i n bands (35). Yamamoto and Konno observed a new p r o t e i n i n l e a f l e t s of the potato p l a n t 6 hr a f t e r i n o c u l a t i o n w i t h an incompatible race of P_. i n f e s t a n s (36). I t i s p o s s i b l e that the incompatible i n t e r a c t i o n r e s u l t s i n the i n d u c t i o n of enzymes not normally present i n the tuber and that such enzymes are the new, observable p r o t e i n s . Further work i s needed to determine the r o l e , i f any, of such proteins i n resistance.


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Potato

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Host


Elicitors C e l l - f r e e fungal preparations that i n i t i a t e an incompatible response i n host t i s s u e have been r e f e r r e d to as e l i c i t o r s or i n d u c e r s . S o n i c a t i o n of P^. i n f e s t a n s mycelia y i e l d s c e l l - f r e e , autoclavable preparations that i n i t i a t e a t y p i c a l incompatible response, i n c l u d i n g terpenoid production and n e c r o s i s , when a p p l i e d to potato tuber s l i c e s . Varns et a l . (37) found that sonicates of both compatible and incompatible races of _P. i n f e s t a n s produced an incompatible response when a p p l i e d to tuber t i s s u e . Glucans i s o l a t e d from Phytophthora megasperma v a r . sojae, a fungal p a r a s i t e of the soy bean p l a n t , were reported by Ayers et a l . to i n i t i a t e an incompatible response i n host t i s s u e s (38). Albersheim and Anderson-Prouty suggested that e l i c i t o r s are carbohydrate-containing molecules f o r which r e c e p t o r s i t e s e x i s t on the plasma membrane of host c e l l s (6). They f u r t h e r conjectured that the s p e c i f i c i t y of the receptor s i t e f o r i t s "matching ' carbohydrate e l i c i t o r may be the b a s i s f o r incompatible i n t e r a c t i o n s as the phenotypic expression of v e r t i c a l r e s i s t a n c e . In other words, receptor s i t e s and e l i c i t o r s may represent the g e n e t i c a l l y determined primary r e c o g n i t i o n f a c t o r f o r a potato v a r i e t y and an incompatible race of _P. i n f e s t a n s . In a recent study, Kota and S t e l z i g demonstrated that prepa r a t i o n s which a c t as e l i c i t o r s caused membrane d e p o l a r i z a t i o n of potato p e t i o l e c e l l s i n l e s s than 1 min f o l l o w i n g exposure (39). These preparations were a s o n i c a t e , a 3-1,3-glucan, and a l i p o p o l y s a c c h a r i d e ( a l l obtained from P_. i n f e s t a n s ) and a p r e p a r a t i o n from ]P. megasperma. Among e i g h t other carbohydrates which are not e l i c i t o r s , only p e c t i n produced d e p o l a r i z a t i o n . This r e p o r t i s supportive of the e l i c i t o r theory of Albersheim and AndersonProuty (6) and the mechanism of a c t i o n of f u n g a l phytotoxins advanced by S t r o b e l (40). In c o n t r a s t to the theory of Albersheim and Anderson-Prouty (6), Ward and S t o e s s l proposed that a r e c o g n i t i o n mechanism (or i n c o m p a t i b i l i t y suppression mechanism) i s i n v o l v e d i n an i n t e r a c t i o n between molecules produced by the fungus and the compatible host (41). M e t l i t s k i i et a l . added another dimension to s p e c u l a t i o n about the incompatible i n t e r a c t i o n by proposing that the potato host produces compounds which induce the formation of compounds by P_. i n f e s t a n s which i n turn induce the incompatible i n t e r a c t i o n i n the host c e l l (42). Keen r e f e r r e d to the e l i c i t o r phenomenon as a derepression of the production of an a n t i f u n g a l compound i n the soy bean host c e l l (43). More work o b v i o u s l y i s needed to determine the nature of the primary events that d e t e r mine c o m p a t i b i l i t y or i n c o m p a t i b i l i t y between host and fungal parasite. 1


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PESTS


The P h y t o a l e x i n Theory Potato tuber t i s s u e i n o c u l a t e d with an incompatible race of Ζ.· i n f e s t a n s was reported to d i s p l a y an incompatible i n t e r a c t i o n when l a t e r i n o c u l a t e d with a normally compatible race (44). This observation l e d to the "phytoalexin theory" (45), which holds that f u n g i t o x i c compounds, p h y t o a l e x i n s , are produced by host c e l l s as a r e s u l t of i n v a s i o n by an incompatible fungus. Kud and C u r r i e r (8) r e c e n t l y reviewed p h y t o a l e x i n s t u d i e s , most of which were conducted with members of the f a m i l i e s Solanaceae (mainly the potato) and Leguminosae. For the potato, the compounds shown i n F i g . 2 are o f t e n r e f e r r e d to as phytoalexins and most of them have demonstrated f u n g i t o x i c p r o p e r t i e s . The f u n g i t o x i c i t y of r i s h i t i n , phytuberin, l u b i m i n , katahdinone, and dehydrokatahdinone was t e s t e d against m y c e l i a l growth of 1?. i n f e s t a n s by Beczner and Ersek (46). At l e v e l s of 25 to 100 ppm i n s o l i d media i n P e t r i d i s h e s , a l l of the compounds e x h i b i t e d moderate to strong i n h i b i t o r y e f f e c t s toward the f u r t h e r spread of 7-day-old c u l t u r e s of P_. i n f e s t a n s t r a n s f e r r e d to the media. Ward et_ a l . (47) reported s i m i l a r i n h i b i t i o n of m y c e l i a l growth with somewhat lower l e v e l s of r i s h i t i n . Ger mination of P_. i n f e s t a n s zoospores was a l s o i n h i b i t e d by s i m i l a r l y low amounts of phytuberin (48), lubimin (49), and r i s h i t i n (50, 51). Since the l e v e l s of phytoalexins able to i n h i b i t pathogen growth i n v i t r o are a t t a i n e d i n many incompatible i n t e r a c t i o n s , i n v e s t i g a t o r s have suggested that phytoalexins p l a y an important r o l e i n i n h i b i t i n g fungal i n v a s i o n (6, 52-57). However, u l t r a s t r u c t u r a l s t u d i e s ( c i t e d l a t e r ) i n d i c a t e observable d i f f e r e n c e s between the compatible and incompatible i n t e r a c t i o n s w e l l i n advance of the production of d e t e c t a b l e l e v e l s of p h y t o a l e x i n s . T h i s does not disprove the theory, s i n c e no one has yet determined the time of appearance or c o n c e n t r a t i o n of phytoalexins i n the microenvironment of the i n d i v i d u a l host c e l l . Conversely, the proof of the theory would r e s t i n determining that phytoalexins are present i n s u f f i c i e n t q u a n t i t i e s e a r l y enough i n the i n f e c t e d , incompatible c e l l to i n h i b i t fungal i n v a s i o n and i n i d e n t i f y i n g the mechanism of i n h i b i t i o n . Hohl and S t o s s e l speculated that phytoalexins i n h i b i t fungal glucanases necessary f o r both f u n g a l growth and d i s r u p t i o n of 0-1,3-glucan b a r r i e r s i n the host c e l l (58). U l t r a s t r u c t u r a l Studies The compatible and incompatible i n t e r a c t i o n s between P^. i n f e s t a n s and potato host c e l l s have been s t u d i e d by scanning e l e c t r o n microscopy and transmission e l e c t r o n microscopy to y i e l d information complementary to biochemical s t u d i e s . Using a scanning e l e c t r o n microscope, Jones et a l . (59) noted sharp boundaries between obviously i n f e c t e d c e l l s near the s u r f a c e and u n i n f e c t e d c e l l s below the s u r f a c e i n the compatible i n t e r a c t i o n



4.

BILLS


Potato

Host

55

of P_. i n f e s t a n s with potato tuber t i s s u e . In t h i s i n t e r a c t i o n , hyphae penetrated i n t e r c e l l u l a r l y deep i n t o the t i s s u e where i n t a c t , l i v e potato c e l l s remained to support the colony with n u t r i e n t s . A sharp boundary between n e c r o t i c c e l l s and l i v e c e l l s was not observed i n the incompatible i n t e r a c t i o n . In e l e c t r o n microscopy s t u d i e s of the i n f e c t i o n of potato l e a f c e l l s , Shimony and F r i e n d (60) observed p e n e t r a t i o n of host c e l l s by P^. i n f e s t a n s hyphae i n both compatible and incompatible i n t e r a c t i o n s . Although the r a t e of i n i t i a l p e n e t r a t i o n d i d not d i f f e r , they reported v i s i b l e u l t r a s t r u c t u r a l d i f f e r e n c e s between the compatible and incompatible i n t e r a c t i o n s 7 hr a f t e r i n o c u l a t i o n (with p e n e t r a t i o n o c c u r r i n g as l a t e as 4-1/2 to 6-1/2 hr a f t e r i n o c u l a t i o n ) . Between 9 and 12 h r , host c e l l s surrounding the s i t e of i n f e c t i o n on the incompatible v a r i e t y appeared to be dead and fungal hyphae were contained w i t h i n the n e c r o t i c area; a t 24 hr, s e v e r e l y damaged hyphae were observed; a f t e r 48 h r , there were no d e t e c t a b l e l i v i n g c e l l s of e i t h e r fungus or host i n the small l e s i o n . An observed f e a t u r e of both the compatible and incompatible i n t e r a c t i o n s was the formation of a sheath or encaps u l a t i o n surrounding the i n t r a c e l l u l a r hyphae. In a p a r a l l e l u l t r a s t r u c t u r a l study of the incompatible i n t e r a c t i o n between l e t t u c e (Lactuca s a t i v a ) l e a f t i s s u e and a f u n g a l p a r a s i t e (Bremia l a c t u c a e ) , Maclean et_ a l . (61) a l s o observed that death of penet r a t e d host c e l l s preceded the c e s s a t i o n of growth and death of fungal c e l l s by s e v e r a l hours. Hohl and S t o s s e l (58) a l s o reported that f u n g a l hyphae penet r a t e d potato tuber host c e l l s i n both the compatible and incomp a t i b l e i n t e r a c t i o n s . The type of e n c a p s u l a t i o n d e s c r i b e d by Shimony and F r i e n d (60) was observed i n both incompatible and compatible i n t e r a c t i o n s and was r e f e r r e d to as an e x t r a h a u s t o r i a l matrix. Hohl and S t o s s e l , however, reported that the t y p i c a l haustorium found i n the incompatible tuber host c e l l d i f f e r e d from that of the compatible host c e l l by the presence of an a d d i t i o n a l e n t i t y , w a l l a p p o s i t i o n s , which surrounded and encased the haustorium and the e x t r a h a u s t o r i a l matrix. The encasement of h a u s t o r i a has a l s o been reported f o r the incompatible, but not the compatible, i n t e r a c t i o n of Uromyces p h a s e o l i v a r . vignae with host c e l l s of the cowpea (62). In two a d d i t i o n a l s t u d i e s of a Phytophthora pathogen i n compatible and incompatible i n t e r a c t i o n s , the presence of w a l l a p p o s i t i o n s was not reported (63, 64). In s t u d i e s of l e a f t i s s u e of the same two potato v a r i e t i e s employed i n tuber t i s s u e s t u d i e s by Hohl and S t o s s e l (58), Hohl and Suter (65) found that h a u s t o r i a i n both the compatible and incompatible i n t e r a c t i o n s were s i m i l a r and were always surrounded by an e x t r a h a u s t o r i a l matrix and sometimes a l s o by w a l l a p p o s i t i o n s . As a p o s s i b l e explanation f o r the marked u l t r a s t r u c t u r a l d i f ferences i n h a u s t o r i a observed between the two types of tubers but not i n the l e a f t i s s u e s , the authors pointed out that the l e a f l e t s of the two v a r i e t i e s d i f f e r l e s s i n r e s i s t a n c e than the corresponding tubers. Various types of f u n g a l i n v a s i o n of potato l e a f c e l l s



56

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RESISTANCE T O PESTS

ranging from hyphae which penetrated c e l l s and then emerged a t another p o i n t to f u l l y developed h a u s t o r i a were observed by Hohl and Suter. Various degrees of h a u s t o r i a l encasement were a l s o observed as shown i n F i g . 3, and the authors suggested that host c e l l r e s i s t a n c e may be r e l a t e d to the degree of encasement that takes p l a c e . They f u r t h e r noted that hyphae enter the l e a f p r i m a r i l y through stomata but are a l s o a b l e to penetrate epidermal c e l l s or h a i r c e l l s . In the incompatible i n t e r a c t i o n , the p a r a s i t e d i d not penetrate deeply i n t o the host t i s s u e and r a r e l y developed s u f f i c i e n t l y to produce sporangia. While u l t r a s t r u c t u r a l s t u d i e s of compatible and incompatible i n t e r a c t i o n s of IP. i n f e s t a n s with the potato host are not i n complete agreement, common f i n d i n g s have emerged: c e l l penetrat i o n occurs i n both circumstances; i n the incompatible i n t e r a c t i o n , p e n e t r a t i o n occurs to a depth of very few c e l l s followed by death of the host c e l l s and l a t e r death of the f u n g a l c e l l s . Conclusion C e r t a i n aspects of the incompatible i n t e r a c t i o n between P_. i n f e s t a n s and the potato host seem to be reasonably well-documented. A number of compounds w i t h demonstrated f u n g i t o x i c i t y are produced when tuber t i s s u e i s invaded, host c e l l s become n e c r o t i c and f u n g a l c e l l s l a t e r d i e . I d e n t i c a l symptoms i n tuber host c e l l s can be i n i t i a t e d by the a p p l i c a t i o n of c e l l - f r e e preparations of the fungus. However, the observed symptoms of i n c o m p a t i b i l i t y may be f a r removed from the primary event that t r i g g e r s the sequence of known events. The f a c t that f u n g i t o x i c compounds are evolved i s not complete proof that they are, indeed, the cause of incomp a t i b i l i t y i n the complex c e l l - c e l l i n t e r a c t i o n . Gene-for-gene i n t e r a c t i o n s between host and p a r a s i t e can be s y s t e m a t i c a l l y tabulated, but only i n the e m p i r i c a l terms of compatible or incomp a t i b l e . The phenotypic mechanisms i n v o l v e d i n i n t e r a c t i o n s a t the c e l l and molecular l e v e l s remain to be d e s c r i b e d . E l u c i d a t i o n of the molecular b a s i s f o r the s p e c i f i c i t y e x h i b i t e d i n gene-forgene, host-pathogen i n t e r a c t i o n s i s w i t h i n reach and i s an important o b j e c t i v e . Although v a l u a b l e i n f o r m a t i o n has been gained through s t u d i e s with tuber t i s s u e , i t appears that a d d i t i o n a l s t u d i e s w i t h f o l i a r t i s s u e should be emphasized. Phenomena observed i n i n t e r a c t i o n s of P_. i n f e s t a n s w i t h s l i c e d or otherwise d i s r u p t e d tuber t i s s u e cannot be assumed to occur i n f o l i a r t i s s u e . Since r e s i s t a n c e to _P. i n f e s t a n s must be expressed i n the f o l i a r p o r t i o n of the potato p l a n t i n order to break the c y c l e of i n f e c t i o n shown i n F i g . 1, i t i s of primary importance to d e s c r i b e and understand r e s i s t a n c e i n terms of the l e a f l e t s r a t h e r than the tubers. Great emphasis has been placed on understanding v e r t i c a l r e s i s t a n c e i n the potato, while h o r i z o n t a l r e s i s t a n c e has r e c e i v e d comparatively l i t t l e study. Since v e r t i c a l r e s i s t a n c e i s temporary and e f f e c t i v e only u n t i l a new race of P_. i n f e s t a n s capable of



4.

BILLS

Phytophthora Infestans and Potato

Host

Canadian Journal of Botany

Figure S. Diagram of haustorial development of Phytophthora infestans on potato leaves, (a) Early penetration of host wall with incipient extrahaustorial matrix formation between host wall and host plasmalemma (hp), (b) Haustorium ensheathed by extrahaustorial matrix and collared by wall appositions at its neck, (c) Progressive encasement of haustorium (ha) by wall appositions (wa). The host plasma membrane (hp) may double-over on itself at the interface of the extrahaustorial matrix (ema) and the wall apposition, (d) Fully encased haustorium with compressed extrahaustorial matrix. Haustorial development may terminate at (b), (c), or (d), probably reflecting rising degrees of host cell resistance (65).


57


58

HOST PLANT RESISTANCE TO PESTS bypassing the resistance mechanism evolves, additional studies aimed at identifying the physical and chemical features of the potato that contribute to horizontal resistance seem in order. Despite the extensive efforts that have been devoted to breeding potato varieties resistant to P_. infestans, potato growers must rely heavily on the use of fungicides to control late blight. Environmental and economic considerations discourage the continued use of conventional fungicides and encourage further research to understand the chemical basis for potato plant re sistance to P_. infestans. Robinson (1), critical of the unholistic approach to disease resistance, pointed out that the disciplines involved have concentrated too heavily upon their particular interests. Effective teams that include plant breeders, plant pathologists, microscopists, and chemists will probably have the greatest impact in the further conceptualization of resistance and the practical application of the concepts to the development of varieties with improved resistance. Literature Cited 1. Robinson, R. A. "Plant Pathosystems," pp 15-54, SpringerVerlag, Berlin, Heidelberg, New York, 1976. 2. Burton, W. G. "The Potato," pp 97-107, 248-253, H. Veenman and Zonen, Ν. V., Wageningen, Holland, 1966. 3. Plank, J. E., van der. "Principles of Plant Infection," p 216, Academic Press, New York-London, 1975. 4. Plank, J. E., van der. "Plant Diseases. Epidemics and Control," p 349, Academic Press, New York-London, 1963. 5. Day, P. R. "Genetics of Host-Parasite Interaction," p 238, W. H. Freeman and Co., San Francisco, 1974. 6. Albersheim, P., and Anderson-Prouty, A. J., Ann. Rev. Plant Physiol. (1975) 26, 31-52. 7. Black, W., Mastenbroek, C., Mills, W. R., and Peterson, L. C., Euphytica (1953) 2, 173-178. 8. Kuć, J., Currier, W. "Mycotoxins and Other Fungal Related Food Problems," Advances in Chemistry Series 149, pp 356-368, American Chemical Society, Washington, D.C., 1976. 9. Sakuma, T., and Tomiyama, Κ., Phytopathol. Soc., Jap. (1967) 33, 48-58. 10. Kuć, J., Henze, R. E., and Ullstrup, A. J., J. Amer. Chem. Soc. (1956) 78, 3123-3125. 11. McKee, R., Ann. Appl. Biol. (1955) 43, 147-148. 12. Locci, R., andKuć,J., Phytopathology (1967) 57, 1272-1273. 13. Korableva, N. P., Morozova, Ε. V., and Metlitskii, L. V., Dokl. Akad. Nauk SSSR (1973) 212, 1000-1002. 14. Clarke, D. D., Phytochemistry (1969) 8, 7. 15. Clarke, D. D. and Baines, P. S., Physiol. Plant Pathol. (1976) 9, 199-203. 16. Zacharius, R. M., Osman, S. F., Heisler, E. G., and Kissinger, J. C., Phytopathology (1976) 66, 964-966.



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17. Tomiyama, K., Sakuma, T., Ishizaka, Ν., Sato, Ν., Katsui, Ν., Takasugi, Μ., and Masamune, T., Phytopathology (1968) 58, 115-116. 18. Katsui, N., Murai, Α., Takasugi, M., Imaizumi, Κ., and Masamune, T., Chem. Commun. (Sect. D) (1968), 43-44. 19. Katsui, N., Matsunaga, Α., Imaizumi, Κ., and Masamune, T., Tetrahedron Lett. (1971) No. 2, 83-86. 20. Katsui, N., Matsunaga, Α., Imaizumi, K., and Masamune, T., Bull. Chem. Soc. Jap. (1973) 45, 2871-2877. 21. Varns, J., Kuć, J., and Williams, Ε. B., Phytopathology (1971) 61, 174-177. 22. Hughes, D. L., and Coxon, D. T., J. Chem. Soc., D. (1974), 822-823. 23. Metlitskii, L. V., Ozeretskovskaya, O. L., Chalova, L. I., Vasyukova, Ν. I., and Davydova, Μ. Α., Mikol. Fitopatol. (1971) 5, 263-271. 24. Stoessl, Α., Strothers, J. B., and Ward, E. W. B., J. Chem. Soc., D. (1974), 709-710. 25. Katsui, N., Matsunaga, Α., and Masamune, T., Tetrahedron Lett. (1974) No. 51-52, 4483-4486. 26. Kalan, Ε. B., and Osman, S. F., Phytochemistry (1976) 15, 775-776. 27. Coxon, D. T., Price, K. R., Howard, B., Osman, S. F., Kalan, Ε. Β., and Zacharius, R. M., Tetrahedron Lett. (1974) No. 34, 2921-2924. 28. Metlitskii, L. V., Ozeretskovskaya, O. L., Vasyukova, Ν. I., Davydova, Μ. Α., Savel'eva, O. H., and D'yakov, Yu, T., Mikol. Fitopatol. (1974) 8, 42-49. 29. Zacharius, R. M., Osman, S. F., Kalan, Ε. Β., and Thomas, S. R., Proc. Am. Phytopath. Soc. (1974) 1, 63. 30. Lyon, G. D., Physiol. Plant Pathol. (1972) 2, 411-416. 31. Lyon, G. D., Lund, B. M., Bayliss, C. E., and Wyatt, G. M., Physiol. Plant Pathol. (1975) 6, 43-50. 32. Beczner, J., and Lund, B. M., Acta Phytopathologica Academiae Scientiarum Hungaricae (1975) 10, 269-274. 33. Metlitskii, L. V., D'yakov, Yu. T., Ozeretskovskaya, O. L., Yurganova, L. Α., Chalova, L. I., and Vasyukova, Ν. I., Izvestiya Akad. Nauk SSSR, Ser. Biol. (1971), 399-407. 34. Zacharius, R. M., Kalan, Ε. B., Osman, S. F., and Herb, S. F., Physiol. Plant Pathol. (1975)6,301-305. 35. Tomiyama, Κ., and Stahmann, M. Α., Plant Physiol. (1964) 39, 483-490. 36. Yamamoto, M., and Konno, K., Plant and Cell Physiol. (1976) 17, 843-846. 37. Varns, J. L., Currier, W. W., and Kuć, J., Phytopathology (1971) 61, 968-971. 38. Ayers, A. R., Ebel, J., Valent, B., and Albersheim, P., Plant Physiol. (1976) 57, 760-765. 39. Kota, D. Α., Stelzig, D. Α., Proc. Am. Phytopathol. Soc. (1977) 4, in press.


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40. Strobel, G. Α., Scientific American (1975) 232, 81-88. 41. Ward, E. W. B., Stoessl, Α., Phytopathology (1976) 66, 940941. 42. Metlitskii, L. V., D'yakov, Yu. T., and Ozeretskovskaya, O. L., Biol. Abs. (1974) 58, No. 5, 2978. 43. Keen, N. T., Science (1975) 187, 74-75. 44. Müller, Κ., and Borger, H., Arb. Biol. Reichsanst. Land Forstwirt, Berlin (1940) 23, 189-231. 45. Müller, Κ., and Behr, L., Nature (1949) 163, 498-499. 46. Beczner, J., and Érsek, T., Acta Phytopathologica Academiae Scientiarum Hungaricae (1976) 11, 59-64. 47. Ward, E. W. B., Unwin, C. Η., and Stoessl, Α., Can. J. Botany (1974) 52, 2481-2488. 48. Varns, J. L. "Biochemical Response and its Control in the Irish Potato (Solanum tuberosum) -Phytophthora infestans Interactions," Ph.D. Thesis, Purdue University, Lafayette, Indiana, 1970. 49. Metlitskii, L. V., and Ozeretskovskaya, O. L., Fitoalexini. Akad. Nauk, SSSR, Nauka, Moskva, pp 176, 1973. 50. Tomiyama, Κ., Ishizaka, N., Sato, N., Masamune, T., and Katsui, N. "Biochemical Regulation in Diseased Plants or Injury," pp 287-292, Phytopath. Soc., Japan, Tokyo, 1968. 51. Ishizaka, N., Tomiyama, Κ., Katsui, N., Murai, Α., and Masamune, T., Plant Cell Physiol. (1969) 10, 183-192. 52. Keen, N. T., Physiol. Plant Pathol. (1971) 1, 265-275. 53. Rahe, J. E., Kuć, J., Chuang, C. M., and Williams, Ε. B., Neth. J. Plant Pathol. (1969) 75, 58-71. 54. Sato, N., Kitazawa, Κ., and Tomiyama, Κ., Physiol. Plant Pathol. (1971) 1, 289-295. 55. Skipp, R. Α., Physiol. Plant Pathol. (1972)2,357-374. 56. Bailey, J. Α., and Deverall, B. J., Physiol. Plant Pathol. (1971) 1, 435-439. 57. Frank, J. Α., and Paxton, J. D., Phytopathology (1970) 60, 315-318. 58. Hohl, H. R., and Stossel, P., Can. J. Bot. (1976) 54, 900912. 59. Jones, S. B., Carroll, R. J., and Kalan, Ε. B. "Scanning Electron Microscopy, Part 2, Proceedings of the Workshop on Scanning Electron Microscopy and the Plant Sciences," pp 397404, IIT Research Institute, Chicago, Illinois, 1974. 60. Shimony, C., and Friend, J., New Phytol. (1975) 74, 59-65. 61. Maclean, D. J., Sargent, J. Α., Tommerup, I. C., and Ingram, D. S., Nature (1974) 249, 186-187. 62. Heath, M. C., and Heath, I. B., Physiol. Plant Pathol. (1971) 1, 277-287. 63. Klarman, W. L., and Corbett, Μ. Κ., Phytopathology (1974) 64, 971-975. 64. Hanchey, P., and Wheeler, Η., Phytopathology (1971) 61, 33-39. 65. Hohl, H. R., and Suter, Elisabeth, Can. J. Bot. (1976) 54, 1956-1970.


Interactions between Phytophthora Infestans and Potato Host

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