Ann. Rep. Phytopathol 198a 18:463�9 Copyright ® 1980 by Annual Repiews Inc. All rights reserved

THE BIOLOGY OF STRIGA� OROBANCHE� AND OTHER ROOT-PARASITIC WEEDS

Lytton J. Musselman

Department of Biological Sciences, Old Dominion University, Norfolk, Virginia 23508

INTRODUCTION

.3743

This review deals with higher plants that are parasitic on the roots of other higher plants. These unique organisms in the genera Striga and Orbanche, are both weeds and parasites. As weeds they show great phenotypic plas­ticity, wide environmental tolerance, prefer permanently disturbed habitats, and are part of a plant guild associated with colonizing or crop complex species. As parasites, they depend upon another vascular plant for food or water, which flows from host to parasites through haustoria. These struc­tures form a morphological and physiological graft with the roots or other underground parts of the host. The remainder of the root system of these parasites is usually condensed and lacks typical root hairs and root caps. All species of Orobanche and most Striga are obligate parasites-they will not develop at all without a host. Facultative parasites such as most of the parasitic species in the Scrophulariaceae are not nutritionally dependent on a host plant but they are invariably attached to one in nature.

Root parasitism is found in the following diverse dicotyledon families of seed plants: Hydnoraceae, Balanophoraceae, Krameriaceae, Lennoaceae, Santalaceae (and segregate and allied families), Scrophulariaceae, and Oro­banchaceae (88, 176). No parasitic monocots are known and there is only one parasitic gymnosperm, Parasitaxus ustus; this organism is endemic to New Caledonia-it has an unique host-parasite interface involving a graft­like union of tissue (L. J. Musselman, unpublished).

463 0066-4286/80/0901-0463$01.00

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464 MUSSELMAN

Inclusion of a review on parasitic weeds in Annual Review of Phytopa­thology attests to a growing awareness among plant pathologists of these important plant pathogens. I attribute this increased awareness to three primary factors. First, the discovery of a witchweed (Striga asiatica ) in the Carolinas in the late 1950s followed by the characterization and synthe­sis of a germination stimulant, strigol, as well as the use of ethylene as a tool in witchweed management. Second, the disastrous drought of 1968-1973 in Sub-Saharan Africa brought attention to the Striga problem be­cause S. hermonthica is a serious pathogen on grains cultivated by subsistence farmers in that region. Third, more books on parasites have appeared within the past two decades than ever befo�e (10,67,88, 176, 182). As a result, parasitic higher plants are being considered in basic studies of cell recognition (22,63), population biology (148), and crop breeding (154).

Except for the book by Beilin (10), the literature on parasites of agricul­tural importance is immersed in the general body of work on parasitic angiosperms. Danger's book, written in the 17th century, is perhaps the first treatment of parasitic weeds as agricultural pests (29) although earlier in the same century they were recognized as pathogens (179). More recently, Parker reviewed the overall Striga problem (122). A comprehensive bibliog­raphy of Striga including lists of hosts was prepared by McGrath et al (102). Reviews on Orobanche (79) and the Orobanchaceae (135), have been pub­lished in recent years. In addition, a series of bibliographies on Striga, Orobanche, and other parasitic weeds is being produced by the Weed Research Organization at Oxford, England. Two volumes based on sym­posia have been published (46, 110). Other useful bibliographic sources are contained in references (67, 81). Illustrations of most species discussed in this paper may be found in (10, 53, 67, 81, 88, 108, 109, 186).

STRIGA AND OROBANCHE

I am departing from convention in treating these two genera together, but in doing so I hope to emphasize similarities in their biology, recent research findings, and some areas that need more research. When relevant, references to other root parasites are incl�ded.

The name Orobanche is from the Greek, orobos, meaning vetch and anchein, meaning to strangle. The modern Arabic name for Orobanche is similar, el halouk, the strangler. This seems to be a more sensible common name than broomrape, a historically sound but misleading common name when applied to the entire genus, since only some species attack broom (Genista). In ancient Greece Orobanche was known as a parasite of crops. Dioscorides (34) described an Orobanche that "chokes pulse," probably a reference to O. crenata, a widespread species that attacks legumes in the

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BIOLOGY OF STRIGA AND OROBANCHE 465

Mediterranean area. According to him, the stalks can be eaten as a potherb similar to asparagus, a fact not widely appreciated by asparagus fanciers.

Striga is from the Latin, striga, a witch, and most species are known by the common name witchweed although that name is also applied to the related genus Alectra. This is a logical name because the parasite "bewit­ches" its host before it emerges and becomes visible above ground. The Latin word striga also refers to a row of grain that has been cut down, likewise an appropriate term in view of its damage to grains.

Striga is often described as a genus of 50-60 species but a figure of 25 may be more realistic. All species that I have examined are annual plants although sometimes they are referred to as perennial. The genus is charac­terized by opposite leaves and irregular flowers with a pronounced bend in the corolla tube. The flowers are pink, red, white, purple, or yellow. There is considerable variation in flower color in both S. asiatica and S. gesneri­oides.

The most studied species of Striga are those of greatest economic im­portance: S. hermonthica, S. asiatica, and S. gesnerioides. Table 1 con­tains a list of synonyms, the geographical range, and some hosts of Striga species.

Unlike Striga, Orobanche plants lack chlorophyll and are fleshy with scale-like leaves and less colorful flowers. Striga is entirely Old World and tropical whereas Orobanche is more widespread-occurring in both tem­perate and semitropical regions. The taxonomy of the broomrapes is more confused than that of the witchweeds with estimates of the number of Orobanche species as high as 150. Species of Orobanche that attack eco­nomic host plants are also listed in Table 1.

Because broomrape species are widely distributed in the north temperate regions of the developed world, a greater number of Orobanche species have been studied than of Striga. On the other hand, Striga is a more serious agricultural problem because it attacks grain crops in areas where few other food crops can be grown. There appears to be little basis for the suggestion that infestations of Striga are correlated with exhaustion of the soil (9).

Seeds and Germination The life history of Striga and Orobanche reflects the specialization of the parasitic mode, e. g. host recognition, early penetration. The first stage is commonly called after-ripening or post-harvest ripening. Little precise data on after-ripening are available. This ripening is the period of time between shedding of the seeds of witchweeds and broomrapes and the second stage conditioning. Necessary time for conditioning is several weeks following after-ripening, during which certain environmental conditions involving water and temperature must prevail before the seeds will respond to a

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Table 1 Striga and Orobanche species of economic importance

Name and synonym

Striga hermonthica (Del.) Benth.3,b

S. senegalensis Benth.

S. asiatica (1.) Kuntzed,e

S. lutea Lour.

S. hirsuta Benth. S. coccinea Benth.

S. gesnerioides (Willd.)

Vatke

S. orobanchoides Benth.

S. curviflora Benth.

S. parviflora Benth.

S. latericea Vatke

S. densiflora Benth.

S. forbesii Benth.

S. aspera (Willd.) Benth.

S. euphrasioides Benth.

S. angustifolia (Don)

Saldhana

Geographic area

Africac

Africa; Arabia through the Indian subcontinent

to China, Indonesia, and the Philippines; USA

(Carolinas)

Africa, India; USA (Florida)

Australia

Australia

Ethiopia

India

East Africa

Africa

India

Major crop host (s)

Millet, sorghum, rice,

maize

Millet, sorghum, rice,

maize, sugarcane

Cowpea, tobacco,

sweet potato

Sugarcane

Sugarcane

Sugarcane

Sorghum, sugarcane

Maize

Sorghum

Sorghum, sugarcane

Selected reference

(36,6 7 , 102)

(67,102,159)

(12,102,109)

(11, 102) (11,102) (49) (67) (186)

(136) (146)

� 0\

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S. barteri Engl. S. brachycalyx Skan.

Orobanche ramosa L. O. mutelii F. W. Schultz

Phelypaea ramosa L. C. A. Mey

O. cernua Loefl. O. cumana Wallr.

O. brassicae Novopokr.

0. crenata Forsk.

O. speciosa DC.

O. minor Smithf,g O. picridis F. W. Schultz

0. aegyptiaca Pers. Phelypea aegyptiaca

(Pers.) Walp.

O. ludoviciana Nutt.h

West Africa

West Africa

Southern and Central Europe; in troduced else­

where, e.g. France, Cuba, Mexico, USA

(California )

Southern Europe and Western Asia

Southern Europe; Mediterranean region

Europe; introduced in New Zealand, US, East

Africa, and perhaps elsewhere

Central southwestern Asia, Middle East

United States

aThe correct spelling as first published by DeIiIe, not hermontheca. bMany species of this gen us were first described as species of Buchnera.

Rice

Sorghum

Tomato, tobacco,

potato, hemp

Sunflower, tobacco

Broadbeans, peas,

lentils

Clover, tobacco

B roadbeans, melons

tobacco

Tomato, tobacco

cReference to this species as introduced (40) and to other species (26) as indigenous to the United States is fallacious. dThe correct name (62) but not universally accepted (e.g. 67). eReports of this species from Australia (163) need verification.

(136) (136) (70)

(l0 , 79, 84 , 90)

(19,51, 184)

(l0 , 72, 79)

(23)

fThe correct author for this species is Smith, not Sutton as is frequently cited. Orobanche minor Smith takes priority. gThis is a most variable taxon broken into 10 taxa in a recent treatment (20). hCollins (23) has recently described (but apparently not validly published) a new species, O. riparia, that appears to be a segregate of O. ludo· viciana.

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468 MUSSELMAN

chemical stimulant from the host. At this time inhibitors may be removed from the seeds (68, 130). This second stage is also known as pretreatment (129). The time necessary for conditioning is remarkably uniform for the various species studied-two weeks for S. hermonthica, S. densijlora, S. gesnerioides (149), Orobanche minor, and O. crenata (40). After condition­ing, seeds germinate in response to a host stimulant (terminal treatment; 130) and the radicle (sometimes referred to as a "germtube" in the Oroban­che literature) emerges. Germination is followed by haustorial initiation and development, attachment to the host root and, lastly, penetration of the vascular tissue. In this chapter emphasis is placed on conditioning and germination.

There are phenolic compounds in the seeds of 11 species of Orobanche that may play a role in seed dormancy (16). Seeds of the host may also contain growth inhibitors that produce differential growth on one side of the parasite radicle, directing growth toward the host (185). On the other hand, some facultative parasites have a negative influence on host root growth (33).

Although some spontaneous germination has been reported in S. asiatica

(68), s. hermonthica (128). O. ramosa (53). and O. cernua (84). most species of Striga and Orobanche require a host root within a few millimeters for germination. O. ludoviciana (187), Aeginetia indica [Orobanchaceae, (92) but see (50)], s. densiflora (67), and S. euphrasioides (181) apparently do not need any host root exudate for germination. Light may inhibit germination of O. ramosa (65).

Determining the chemical makeup of the stimulant has involved numer­ous researchers and laboratories during the past 30 years. With the discov­ery of S. asiatica in the United States a new urgency in this regard was realized. Worsham and others at North Carolina State University discov­ered that several substances, including kinetin and coumarin derivatives, (189) and certain other substituted purines would stimulate germination (189). In 1972 the structure of a stimulant exuded from cotton roots was finally determined (24) and given the name "strigo1." In 1974 the compound was synthesized (61). Strigo1 is extremely active biologically-it promotes germination of seeds of S. asiatica at concentrations as low as Hr16M (61). Johnson began his early investigations of the chemical makeup of the stimulant of O. minor and S. hermonthica in the 194Os. In 1976 he, his colleagues at the University of Sussex began to produce chemical ana­logs of strigol. They reported (75) that several showed great potency in stimulating germination of both Striga and Orobanche at extremely low concentrations. Strigol and the strigol analogs (sometimes known as "GR compounds" after Rosebery who worked in Johnson's laboratory) are char­acterized by one or more unsaturated lactone rings.

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BIOLOGY OF STRIGA AND OROBANCHE 469

We know considerably less about the compounds that stimulate germina­tion of Orobanche although strigol and strigol analogs may effect germina­tion. For example, concentrations of 0. 1 to 1 ppm of GR will cause germination of O. ramosa at 25° C (155). Kumar (91) has shown that strigol induces unipolar germination in O. aegyptiaca but in general the relation­ship between radicle morphology, haustorial development, and these stimu­lants remains obscure. The chemical structure of the Orobanche stimulant has not been determined although some evidence suggests that it may be a benzopyran derivative (30, 31).

Other compounds may play a role in stimulating germination of Striga. The most important of these from the standpoint of control is ethylene (43). Ethylene has also been reported to induce germination of Orobanche (21). Reports that various plant tissues and pond and stream water will induce germination of S. asiatica (27) need to be reconsidered in light of the common occurrence of ethylene gas in laboratory situations (167) as well as its release from damaged plant tissues.

Worsham has shown that kinetin will induce germination of S. asiatica without a conditioning period. Van Stadan (180) suggests that Striga germi­nation is mediated by release of cytokinins from maize roots although the interaction of strigol and cytokinins under field conditions has not been in­vestigated. Kinetin inhibits germiniation of Orobanche (1). Gibberellins alone apparently do not stimulate germination of seeds of S. asiatica (191), but will stimulate Orobanche at least in the presence of a host (65, 152). Abdel­Halim et al (1) found that maximum germination of Orobanche takes place in the vegetative phase of the host when gibberellin production is highest.

Still another group of chemicals, coumarin and its derivatives, induce germination. Worsham et al (189) obtained 100% germination in S. asiatica with scopoletin. This is of particular interest since these compounds are well-known allelochemics (140, 150). I know of no evidence that species of Striga and Orobanche might be allelopathic to their hosts-their relation­ship with other plants is usually perceived as simple and direct parasitism. There is a recent report of a very pronounced allelopathic effect by the facultative root parasite Bartsia odontites [Scrophulariaceae (37)].

It is not yet known how these various compounds function in the seeds of root parasites. Much research remains to be done in this regard. Perhaps there is a role for the well-developed aleurone layer in these processes. Egley (42) has shown that puncture of the aleurone layer will induce germination in S. asiatica. A careful histochemical study of this layer during after­ripening and conditioning might elucidate the fate of stimulants within the seed.

The influence of temperature on several species of Striga has been inves­tigated recently. Highest germination was obtained when S. hermonthica was

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470 MUSSELMAN

conditioned at 23° C and for S. asiatica and S. gesnerioides at 34° C. Mter conditioning, S. hermonthica and S. asiatica genninated best at 33° C (149).

Some Host-Parasite Interactions

The effect of the parasite upon the host is both direct and indirect. Water and foodstuffs are removed and stunting and yield reduction occur (17,25). For example, o. cernua in Hungary reduced yield of sunflower by 30% and also lowered the oil content of seeds (172). In sugarcane the stem is weakened (96) and the quality of the juice is reduced by root-parasitic weeds. Similar results have been obtained for fiber crops (53).

Movement of photosynthate from host to parasite is well documented (119, 153). In essence, the parasite becomes a metabolic sink for carbohy­drates produced in the host (96). In a similar study of facultative root parasites, Munteanu (107) found that host plants contained more starch and nonreducing sugars than parasites.

Nitrogen metabolism has also been studied. Younis & Agabawi (192)

showed that S. hermonthica growing on Sorghum vulgare contained 10.5% of the total weight of host and parasite tissue but 24.9% of the total nitrogen. Orobanche cernua and o. aegyptiaca lack threonine/Serine dehy­dratase and are therefore incapable of L-isoleucine synthesis (76, 111). There is a similar report for a hemiparasite (77) and it could be interesting to know if the same is true of Striga. Such a lack would put an additional strain on the nitrogen economy of the parasite and may account, in part, for the apparent nitrogen sink of the parasite. Parasitism by Orobanche also reduces the level of nucleoprotein in the host stem but not root (164) as well as lowering chlorophyll content (165). Application of nitrogen will reduce the production of gennination stimulant in the host (126) and also compensate for lack of gibberellic acids in the host plant (38), again indicat­ing a stress on host nitrogen resources.

Apparently there is a direct relationship between the sugar sink caused by the parasite and nitrogen starvation in the host (83). Nitrogen is usually carried from the roots to the aerial portion of plants in the phloem, but with a drain on sugars less nitrogen can be translocated. As a result, there is a reduction in amino acid synthesis and growth and consequently in sugar production in the host. This in tum means less sugar for the roots, and the cycle is repeated.

Evidence is now available for a more insidious indirect effect of the parasite upon the host. Field observations had long supported the belief that the effect of Striga upon its host involved more than just the removal of water and other nutrients, because the small Striga plant had such a pro-

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BIOLOGY OF STRIGA AND OROBANCHE 471

found effect on the much larger host (179). Experimental evidence for this indirect effect is now available. Working with S. hermonthica on Sorghum vulgare. Drennan & EI-Hiweris (3S) demonstrated that parasitized plants had 90-95% fewer cytokinins and 30-S0% fewer gibberellins than control plants while the concentration of inhibitors (abscissic acid and farnesol) was somewhat increased in parasitized plants. Varieties of sorghum that exhib­ited resistance had higher concentrations of cytokinins than more suscepti­ble varieties. Application of nitrogen partially compensated for lack of gibberellic acids in the sorghum cultivar 'Dobbs'.

Other direct effects of Striga and Orobanche may include the differential absorption of minerals including P, K, S, and Fe (101). Striga hermonthica and O. ramosa can absorb minerals directly into the nonhaustorial portion of their roots (69). Rhinanthus (Scrophulariaceae), a hemiparasite, has been shown to be the most mineral efficient of a group of pasture plants (171).

A strong transpirational pull from host to parasite has been well docu­mented (SS, 144). High humidity will inhibit growth in S. asiatica (41) perhaps due to a reduced flow of materials from host to parasite. Ecologi­cally, Striga and Orobanche (15) and most root parasitic weeds are found in open, sunny habitats that would favor increased transpiration.

The Haustorium and Its Development Kuijt (S9) was correct in his assertion that the haustorium must be at the center of our thinking in parasitic plants. The haustorium is in fact the salient feature of parasitic weeds for it is through this organ that all transfer between host and parasite is achieved as there is no evidence of indirect transfer. A recent review summarizes our knowledge, mainly descriptive, of haustoria (S9). In the short time since that review appeared considerable advances have been made in understanding various physiological aspects of haustoria.

Okonkwo ( lIS) noted that no haustoria were produced by S. hermonthica in sterile culture and cited this as indirect evidence that the stimulus for initiation comes from the host root. That a definite chemical factor might be involved was first recorded by Edwards (40) who termed it a postgermi­nation factor. Recent work on haustorial initiation has centered on faculta­tive parasites but has direct relevance, I believe, for Striga and Orobanche. Atsatt and his students have studied chemical factors in haustorial initia­tion, repression, and haustorial development in terms of whole plant nutri­tion (6). Riopel's work involves the elucidation of the chemical nature of natural host exudates and other compounds that elicit the initiation re­sponse in the root of the parasite. As an experimental organism, Riopel chose a common, somewhat weedy species of facultative parasite, Aga/inis

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472 MUSSELMAN

purpurea (Scrophulariaceae). When this plant was grown in sterile culture, he noted that radicles near the seed coats developed haustoria. Since one of the major components of seed coats are gums he began a search of common vegetable gums for a haustorial initiating factor and found high activity in gum tragacanth. Further work has shed light on the type of chemical involved. Flavonoid compounds such as quercitin, rutin (151), and vanillin (J. Riopels, personal communication) show considerable activ­ity. Gum tragacanth applied to S. asiatica seedlings may elicit a similar response although further work is necessary to document this (115).

As with germination, compounds that show considerable activity are those for which an allelochemic role has been demonstrated (150). Initiation is an exceptionally rapid process. Exposure to the stimulant causes notice­able swelling of cortical cells within 30 min (152).

A recent review (83) of how parasitic angiosperms affect their hosts emphasizes the well-documented phenomenon of xylem-to-xylem linkup of host and parasite without the involvement of typical phloem tissue. How­ever, there is now unequivocal evidence of phloem in the haustorium of an obligate root parasite (35). Although host and parasite phloem exist in close

proximity, parenchyma cells are always interposed. Phloem-like cells have been reported in the haustorium of O. ramosa (132). There is a report of production of haustoria by leaves of Orobanche (183).

If a suitable chemical influence is present, a primary haustorium will develop at the tip of the radicle. This haustorium then becomes appressed to the host root and penetrates it. In S. gesnerioides, the primary haus­torium enlarges to the size of a small pea and the shoot is very small. The seedlings of S. hermonthica and S. asiatica on the other hand resemble more closely the seedlings of a "typical" nonparasitic plant. These three species of Striga are characterized by the production of adventitious roots in the internodes of the young stem beneath the scales. These roots may attach themselves to the same root to which the primary haustorium is attached or more frequently to a nearby root so that in a short time the parasite is connected to many roots. Working with S. gesnerioides, Ba (7) found that the number of adventitious roots and haustoria varies depending on the species of host plant. It is important to emphasize that Striga (in particular) does not weaken but actually strengthens the roots that are parasitized (C. Parker, unpublished). One way in which Striga may accom­plish this is by the stimulation of lignification in host tissue. Striga asiatica and S. hermonthica actually stimulate root production. This phenomenon is particularly evident when attempting to pull up infected and noninfected hosts in the field. The situation is different in Orobanche where adventitious roots, if produced at all, are not prolific. Rather, a swollen area sometimes referred to as a tubercle develops, from which short stubby roots may develop.

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BIOLOGY OF STRIGA AND OROBANCHE 473

Data on biochemical needs for shoot development in Striga are equivo­cal. Striga hermonthica apparently will develop without exogenous hor­mones (118, 120), but hormones are necessary for development in S. asiatica (191). Alectra vogelii (an obligate root parasite; Scrophulariaceae) will also develop in culture without hormones (121). Similar data on Orobanche are not available although the situation in the related Aeginetia indica (50, 173) resembles that of S. hermonthica. Work by Nes et al (113) on an indigenous North American member of the Orobanchaceae, Epifagus virginiana, indi­cates that this holoparasite is capable of producing its own sterols and does not depend upon its hosts for these compounds.

A role for micoorganisms has been discovered in the seedling biology of both Striga and Orobanche. Cezard (17) reported the presence of an endo­phytic fungus in Orobanche. Petzoldt (133) has shown that O. crenata in broadbeans is associated with the bacterial root nodules of that host al­though there is apparently no correlation between germination of broom­rape and host Rhizobium (1). In some California soils Rhizoctonia solani inhibits germination of O. ramosa (55). Of special interest is the report by Zummo (193) of an endogenous bacterium in S. hermonthica that may protect the subterranean parts of seedlings from attack by other microor­ganisms. This work needs verification.

Little information is available on induction of flowering in Striga and Orobanche. It appears that there is no correlation between flowering of the host and the parasite at least in O. minor (85) despite an earlier report to the contrary (66). Garman (53) states that o. ramosa flowered all during the growing season. Striga asiatica and S. gesnerioides will likewise flower regardless of host flowering (L. J. Musselman, unpublished).

Hosts A review of the literature on hosts for Striga and Orobanche provided conflicting data. Most species have a very broad host range, yet there are physiological races within species of broomrapes and witchweeds that have extremely narrow host ranges.

Overall, Orobanche has a much broader host range than Striga, although broomrapes appear to occur most frequently on members of the Fabaceae, Solanaceae, and Asteraceae. Monocots, especially grains, are rarely at­tacked although there is a report of O. cernua on wheat (162). Perhaps O. crenata has the narrowest host range, being restricted more or less to legumes, but carrots are also parasitized. Both O. ramosa (9) and o. cernua appear to be very promiscuous; they have been reported on 27 (171) and 18 different genera (143), respectively. How much these host lists reflect biological reality is debatable. The point seems to be that although broom­rapes overall have a broad host range they may show a preference for certain families.

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With the exception of S. gesnerioides the situation in Striga is different from that in Orobanche. S. gesnerioides has a broad host range of dicots and a few monocots (67). Striga hermonthica, S. asiatica, and other less serious species (Table l) are restricted almost entirely to grasses. This seems natural because these plants are native to savannas, plant communities dominated by grasses. A comprehensive host lists for Striga species may be found in McGrath et al (102).

The existence of strains of witchweed physiologically adapted to certain hosts was first intimated by Lewin in 1932 (98) who suggested that there may be "biological strains" of S. asiatica. King & Zummo (82), among others, recognized a sorghum strain and a millet (Pennisetum american­um) strain of S. hermonthica. This is also true in the Sahel, where pen­nisetum millet is grown mainly in the drier and sorghum in the wetter zones. In the millet zone, this crop is seriously attacked whereas sorghum is immune. Likewise, in the sorghum zone, millet fields are free while sorghum is attacked. We now have a basis for this host specificity. Using seed from both the sorghum and millet strains of S. hermonthica, Parker & Reid (127) conducted reciprocal germination tests using the different hosts and parasite strains. Their results clearly indicate that root exudates play a role in these highly specialized systems. Millet Striga was not stimulated to germinate by sorghum exudate nor was sorghum exudate effective with the millet Striga .

Similar specialization has been recorded for S. asiatica (94) relative to sorghum and millet strains, thus paralleling the situation in S. hermonthica. There were also differences in the biochemistry and weight of the seeds of the two strains (94). This specialization may result in the adapative advan­tage of less intraspecific competition within the speCies (94). Such millet strains are apparently not present in South Africa where pennisetum millet is a trap crop (60).

Host-specific strains of S. gesnerioides are also known. Over much of its range it is best known as a serious parasite of cowpeas. This form is much branched and has blue flowers (109). Another form parasitizes the weedy legume Tephrosia pedicel/ata, is sparsely branched, and has pink flowers (109). It is not known whether these forms, or those of S. hermonthica and S. asiatica, are interfertile. There is evidence that hosts can influence the morphology of the parasite, at least in one facultative root parasite (5) and one wonders whether the same is true in Striga and Orobanche.

There is a parallel host specificity in Orobanche where a turnip strain of O. cernua would not germinate with mustard, nor a mustard strain with turnip (166).

Considerable progress has therefore been made in understanding some mechanisms of host specificity; however, at least one question remains.

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BIOLOGY OF STRIGA AND OROBANCHE 475

Does host recognition operate at several levels? This would appear to be the case as it is well known that many plants that produce germination stimu­lants will not support growth of the parasite. Examples include cotton which produces strigol but does not support S. asiatica. Likewise, flax is often used to germinate O. minor but is not a host. Parker et al (126) have found strains of hosts with both high stimulant production and resistance. Perhaps both the germination stimulant and the haustorial factor play a role in host selection.

There are several reports that S. asiatica and S. hermonthica grow, albeit depauperately, on nongramineous hosts (102,160). This enigma might now be explained in light of the above work. If host recognition acts at several levels, i.e. germination, haustorial initiation, attachment and penetration, physiological compatibility, then some chemical clue may be needed at each stage. Once over the two hurdles of germination and haustorial initia­tion the parasite may be able to attach to plants other than grasses. In the anomalous parasitism of nongraminoids, seeds could have been stimulated to germinate by widespread soil ethylene (167), or other naturally occurring germination stimulants, haustoria induced to develop by a grain crop resi­due with resultant attachment to a surrogate host. Studies of host parasitism in pot culture cannot be meaningful unless the medium is thoroughly washed of plant remains that might exert a chemical influence on the parasite.

Similar evidence is available regarding Orobanche that might support the theory of multilevel host recognition. Using many different hosts, Racovitza (143) established five categories of host selectivity in O. cernua that may represent various steps in host recognition and compatibility: (a) no germi­nation, no attachment, (b) germination but no attachment, (c) germination and attachment, no development, ( d) development to the tubercle stage only, and (e ) parasite maturation.

Biological and OJher Control Means Control methods include herbicides, and mechanical, cultural, and biologi­cal means. In its very broadest sense biological control includes germination stimulants, insects and fungi, trap crops and catch crops, and breeding for resistance. Catch crops are hosts that both stimulate germination and sup­port parasitism (122). Trap crops stimulate germination but do not support parasitism (122). Catch crops are usually plowed under to prevent parasite maturation; this is not necessary for trap crops. Good examples of trap crops are Sudan grass for S. hermonthica (67, 95) and Carum ajowan for O. cernua (142). The latter will induce germination of most of the seeds in the soil. Trap crops for S. asiatica include cotton and peanut (67). Last (95) has discussed the relative merits of trap cropping versus herbicidal control.

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Trap cropping for five weeks decreased the incidence of S. hermonthica but benefits in terms of yield during the first year were greater with 2,4-0.

There is a considerable literature on control with herbicides incorporated into the soil (155), or applied either before or after emergence (123, 138). In general, 2,4-0 (45,95) and related compounds (137) have given very good results although a variety of materials including kerosene have been used (87). In Rhodesia, herbicides have reduced Striga to a minor problem (H. Wild, personal communication). Striga in rice is especially difficult to con­trol (32). Herbicide can be transported from host to parasite but only with resultant host damage (157). In small infestations sterilization of the soil with methyl bromide has proven efficient (187). A novel approach to control in hot dry areas is solar sterilization of the soil using polyethylene film (72). There are conflicting reports of control by grazing. For example, O. minor is controlled by grazing in New Zealand (168), whereas the same species has been reported to kill goats in Egypt (78). These conflicting results may be due to difference in the host chemicals or variation in the parasite.

Use of germination stimulants are now being tested under conditions of peasant farming (117). While ethylene gives excellent control of Striga (45), it is too expensive and requires mechanization which is not usually available in developing countries. Thus, areas where root-parasitic weeds have their greatest impact are the very regions restricted to hand weeding for control. Careful weeding, however, can give significant increases in yields (36, 73).

The potential for biological control of parasitic weeds with insects and some other agents has been reviewed recently by Girling et al (54). They conclude that no effective method of biological control is yet available but urge surveys of related species of parasites in tropical regions where a wide range of insects may be present.

Several insects are known to attack Orobanche. These include the dipt­eran Sciara sp. that eats seedlings and stems of some Orobanche (15). The agromyzid fly, Phytomyza orobanchiae, has long been known to attack species of Orobanche (184). It is widespread and apparently occurs in many locations where Orobanche grows, although not all species are attacked with equal vigor (97). It has been claimed that Orobanche is less of a problem in Yugoslavia as a result of a control program involving Phytomyza (97). Insects that damage tobacco (Spodoptera litura, Heliothes armigera, Myzus persicae ) infected 50%, 63% and 7% of a random sample of 1000 Orobanche plants (species not identified), respectively (86) perhaps as a result of tobacco compounds in the parasite.

Differences in predation by insects might be attributable to the chemical influences of different hosts and/or host strains. Rascol et al (147) found alkaloids in the parasite similar to those of the host. Host chemical influ­ences might help explain the lack of uniformity in infestations in contiguous

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BIOLOGY OF STRIGA AND OROBANCHE 477

areas reported by Girling et al (54). The buffering of the chemical makeup of the parasite by the host must be kept in mind when considering insect predation for biological control.

Breeding for resistance to witch weed is now being undertaken as a prom­ising control for Striga because it can be used under conditions of erratic rainfall, low soil fertility (145), and primitive agriculture. The factors in­volved in the resistance are not all known but no doubt include the various stages of host recognition and compatibility discussed earlier. For example, some strains of sorghum produce little germination stimulant (126) whereas others produce large quantities of stimulant yet are resistant (36, 126). Resistance based on low stimulant production was suggested by Williams (188).

Other factors involved in resistance involve time of maturation of the host relative to infection. In sunflower it has been demonstrated that maximum parasitism takes place when the host plant is young (172). This may be correlated with lignification of the root since older roots are not affected nearly so severely. A similar situation may occur in Aeginetia (99). Other plants that have been screened for resistance include tomatoes [with very little success (2)] and eggplant (28). Apparently the presence of phenolic compounds in hosts has little effect on resistance (80).

Resistance also may be lost as shown by the well documented example of the breakdown of resistance in sunflower to O. cernua in the Soviet Union. In the 1920s strains of sunftower were developed that were resistant to O. cernua. but with time resistance was lost and new host strains were developed. After another 20 years resistance once again was lost as a result of the development of new strains of the parasite which were morphologi­cally identical with one another (139). A similar situation occurred in France for O. ramosa on hemp. As early as 1746 Guettard (56) noted that the parasite damaged hemp. Over two centuries later, Badoy (8) reported that varieties once resistant in the Anjou region of France had become susceptible. He attributed this to loss of resistance by the host although we need not rule out a change in the physiology of the parasite similar to that reported above.

Introduced Parasites In the few notable instances where root-parasitic weeds have been spread globally, they have moved from the Old World to the New. Contrariwise, no New World root-parasitic weeds of any agricultural importance have been introduced to the Old World. The only temperate region where Striga has been spread is in the United States. Two Old World broomrapes O. minor and O. ramosa have been dispersed throughout much of the world.

Certainly the most widely distributed root-parasitic weed is S. asiatica. It probably has become a problem only in the past century. In South Africa

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where it has proved especially virulent it apparently only became a serious pest when new land was planted (131) since it never reached high popula­tions in native grasslands (48). As soon as it became serious in the maize growing regions of South Africa, the US Department of Agriculture issued a warning to American maize growers (47). Over half a century passed before S. asiatica was introduced or, more correctly, discovered in the United States. Pavlista (129) discussed various ideas regarding the introduction of this parasite into the United States including my favorite theory, transport on wool from South Africa.

The witchweed eradication and control program in the United States is the envy of other nations. Major efforts for control and eradication have been reviewed recently (45). The cost of the Striga asiatica control program is estimated at about $6 million per year. When this expense is weighed against the loss to corn and other crops, however, the cost-benefit ratio indicates the value of the program (44).

More recently, S. asiatica has been reported as damaging maize in Thai­land where its spread has been attributed to large-scale mechanized farming and movement of machinery from infested to new areas (175). As late as

1974 S. asiatica was not a problem in Thailand, but within five years it infested over lOOO ha in the northeast portion of that country (174).

In January 1979, S. gesnerioides was verified as occurring in a few coun­ties of central Florida (190). Preliminary tests indicate that it poses little danger to commercial crops with the possible exception of sunflower and sweet potatoes (L. J. Musselman, unpublished).

In contrast to Striga, dispersal of broomrapes in the United States has been over a large geographical and temporal span. The history of O. minor in this country has recently been discussed (51) and has been compared to New Zealand where O. minor is now a serious problem on tobacco and subterranean clover in some areas (71, 168). Orobanche ramosa, a far more serious pathogen of several important crop plants, has a similarly long history in the United States. In his classic paper, Garman (53) suggests that O. ramosa was introduced to Kentucky with hemp although he records it as parasitizing several other hosts of diverse families with less frequency. To my knowledge, the species is no longer extant in Kentucky. Later, and obviously quite independently of the infestation in Kentucky, O. ramosa was found in New Jersey on tomato (58) and later on coleus in a greenhouse on Long Island, New York (106). The most serious infestation in the United States at present is that on tomato in California, which was first reported in 1928 (171). Orobanche ramosa is a serious pathogen of tobacco in Cuba (93) and Mexico, but has not spread extensively.

In the United States O. ludoviciana, one of the several native species of broomrape, robust in habit and widespread, has become a parasite of com-

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BIOLOGY OF STRIGA AND OROBANCHE 479

mercial crops. It was first noted as a parasite of tobacco in Ohio in 1931 (134) and later on tomatoes in Wyoming (169) and California (14).

Where possible, standard techniques of phytosanitation may help control the spread of these parasites. It is known that clean clover seed has re­stricted the spread of O. minor in some situations (100).

OTHER ROOT-PARASITIC WEEDS

Other genera of root-parasitic weeds of agricultural importance are most commonly obligate parasites. I have listed some of these in Table 2, putting special emphasis on recent discoveries. This is far from an exhaustive com­pilation. Perhaps the most damaging is Alectra vogelii, a serious parasite of cowpeas and some other legumes in Africa (186). Related species of Alectra can attack tobacco and other crops (186) and sunflower (c. Parker, personal communication). Two genera of the Orobanchaceae, Aeginetia (92,96) and Christisonia (141), have been reported to damage sugarcane and other crops. Aeginetia appears to have the greatest potential as a pathogen because it will attack several grasses including grain crops such as sorghum, pennisetum millet, and several finger millets (92). It is fortunate that neither Aeginitia or Alectra have been spread.

Facultative parasitic species of the Scrophulariaceae have been impli­cated in localized growth losses but have never reached the importance of Striga and Orobanche. In the American South, Seymeria cassioides has caused mortality of pine seedlings under conditions of water stress (57, 108). Several grassland species reduce yield in grazing meadows. For example, Rhinanthus serotinus has been reported to cause a 25% reduction in biomass as well as a decrease in the numbers of important forage species in Eastern Europe (104). Related genera (e.g. Odontites) are known to cause similar harm.

Care is needed in equating losses in pot culture with field loss (108, 116), especially in facultative parasites with broad host ranges.

Only recently have there been reports of pathogenic species in the Balano­phoraceae,-a tropical family of bizarre obligate holoparasites (88). In Nigeria, Thonningia sanguinea has caused losses in rubber (125) and cacao plantations (J. Swarbrick, personal communication). On rubber, one para­site plant attacked as many as 20 individual host plants. Balanophora indica will parasitize coffee (112) but apparently with little damage. Species of Balanophora have a broad host range including commercial species of Citrus and Ficus (59), but are apparently not serious problems. Only one member of the Hydnoraceae has been reported on a commercial crop, cotton (13), again with insignificant damage.

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Table 2 Some other root parasites known to damage crops

Name Location Host Reference

Santalaceae Thesium humile Yahl Libya, Spain Barley (18, 103) T. australe R. Br. Australia Sugarcane (68a) T. resedoides A. W. Hill South Africa Sugarcane (Fide her-

barium spec-imens, Kew)

Acanthosyris pauloalvimii Brazil Cacao (3) Barr.

Exocarpus bidwillii Labill. Australia Young eucalyptus (74) Osyris alba L. Yugoslavia Grapes (81)

Balanophoraceae Thonningia sanguinea Yah! Nigeria Rubber, Cacao (125) Balanophora indica Wall. India Coffee (59, 112)

Hydnoraceae Prosopanche bonacinae Speg. Argentina Cotton (13)

Scrophulariaceae Alectra vogelii Benth.a Africa Peanuts,cowpeas (186) A. orobanchoides Benth. South Africa Sunflower (C. Parker,

personal com-munication)

A. kirkii Hemsl. Rhodesia Tobacco (186) Rhinanthus serotinus Europe Forage (104)

(Schon.) Oborny Seymeria cassioides Southern US Young pines (57)

(J. F. Gmet) Blake Orobanchaceae

Aeginetia indica L. Java, Philippines, Sugarcane, rice, (92,96 ) Formosa, Japan maize

Christisonia wight;; Elmer Philippines Sugarcane (141)

aThis genus is sometimes split into Melasma Berg. and Alectra Thun.

The Santalaceae are a family of facultative hemiparasites. Of the several species reported to cause significant damage, Thesium is perhaps the most important, with one species in Australia that damages surgarcane (68a) and one in the Mediterranean region that parasitizes cereals ( l8, 103). In Libya, it is estimated that T. humile reduces barley yield by as much as 10% (M. A. Abou-Raya, personal communication). This genus reaches its greatest development in South Africa where over 100 species occur (64). Very recently T. resedoides has been a problem in sugarcane in South Africa (C. Parker, personal communication). One seemingly benign species, T. lino­phyllum, has been introduced into the United States (170).

Considering the large number of plants involved, we should not be sur­prised to find that other species of parasites, both obligate and facultative, have pathogenic potential. Factors responsible for new weed problems in­clude rapid genetic change and a change in cultural practices (124). The

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BIOLOGY OF STRIGA AND OROBANCHE 481

latter would certainly include the clearance of new land and the introduc­tion of new crops into areas already occupied by root-parasitic weeds. It is not hard to find examples of either phenomenon. The pathogenicity of Seymeria cassioides resulted from the use of peripheral sites for forestry. Striga latericea on sugarcane in Ethiopia and A canthosyris pauloalvimii in Brazil are similar examples (Tables 1 and 2). An example involving rapid genetic change would include the situation of Orobanche cernua on sun­flower in the Soviet Union and perhaps Striga gesnerioides on tobacco in Rhodesia.

CONCLUSION

During the past two decades noteworthy progress has been made in under­standing the biology of parasitic weeds. Perhaps most significant is the discovery of strigol and related compounds and ethylene gas as germination stimulants. Although we still do not know how these stimulants effect germination of the seeds, there will be considerable activity during the coming years testing these and similar compounds under field conditions in various regions of the world. In the process we should learn much about their effects on host plants and the environment.

For the first time now, we are able to investigate the component processes of germination and infection such as a consideration of the physiology of haustorial initiation. If it were possible to block development of the first contact with the host, a new control measure might be available. Likewise, further investigations into the mechanisms by which these parasitic weeds affect their host plants may provide means for alleviation of the effects of parasitism under field conditions. I am optimistic that we are entering a new era in understanding these pathogens and that increased basic research will result in new and more effective control measures.

Realistically, however, it will be some time before these methods can be used where parasites cause the greatest impact, in primitive agriculture where the strictures of aridity, low soil fertility, and lack of capital for technological solutions will continue to limit the types of crops and control measures that can be used by subsistence farmers. Under such conditions, hand weeding and hoeing will continue to be the chief means of managing these pathogens.

For these reasons, breeding of resistant varieties of host plants will be the major objective of the international Striga (145) and Orobanche control efforts (F. Basler, personal communication). Care is needed here, however, to avoid the introduction of cultivars of host plants into resistant geograph­ical regions where more covalent strains of these root parasites may be present. Perhaps more emphasis needs to be placed upon resistance through

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tolerance, that is, the ability to produce a good yield despite being parasit­ized.

In addition to consideration of physiological strains, it follows that an investigation should be made of the sources of genetic variation that pro­duces such strains and the inheritance of traits related to parasitism as has been done for some other parasites of pathogens (4). In these two most important genera of root parasites we are dealing with pathogens that are spread solely by seed, yet we know little about factors involved in seed production and dissemination in either Striga or Orobanche. Some prelimi­nary data are available. The genus Orobanche is probably characterized by a very high level of self-fertile flowers (23). Variation in O. crenata involves meiotic aberrations (105). Studies have shown that the American strain of witchweed is autogamous (114). Preliminary evidence indicates that S. hermonthica may be an outcrosser (C. Parker, unpublished). Studies on the floral biology of Striga and Orobanche are vital to understanding variability within species. What are the pollen vectors of these plants? This as well as studies on the interfertility of the various physiological races can be carried out in developing nations.

Coordinated international effort on these parasites should include field surveys to determine the geographical extent of infestations as well as some measure of the economic and human consequences in each nation. This will prove difficult in less developed countries but is necessary to properly assess the impact of root-parastic weeds on agriculture. In the few instances where surveys of any sort have been conducted large losses in yield have been recorded (158, 161).

Lastly, the plant science community, while recognizing federal quaran­tines and the danger posed in handling these pathogens, should have more contact with this group of parasites. Even though these parasites are often included in plant pathology and weed science texts, little has been done to educate the botanical and agricultural public to their danger. One effective

way to do this would be by the distribution of specimens (duly devitalized!) to herbaria so that if one of these parasites should tum up it can be quickly and accurately identified. It has been my experience that some state and regional herbaria lack even a single specimen of Striga.

ACKNOWLEDGMENTS

Comments and suggestions on this manuscript by my fellow strigologists Professors J. L. Riopel and A. D. Worsham, are appreciated. Appreciation is also extended to individuals who brought to my attention various refer­ences. Lastly, I especially value the encouragement and assistance of Mr. C. Parker, Tropical Weeds Specialist, in preparing this review. He also freely provided unpublished information incorporated in this review.

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