Parasitic Plants in Agriculture: Chemical Ecology of Germination and Host-Plant Location as Targets for Sustainable Control: A Review
ABSTRACT Parasitic plants are among the most problematic pests of agricultural crops worldwide. Effective means of control are generally
lacking, in part because of the close physiological connection between the established parasite and host plant hindering efficient
control using traditional methods. Seed germination and host location are critical early-growth stages that occur prior to
host attachment, and provide promising targets for ecologically sound management of parasitic weeds. Knowledge of parasite-host
interactions, particularly chemical cues that induce parasite seed germination and mediate host location, should facilitate
the development of novel management approaches. In parasitic plants that attach to host roots—e.g., Striga and Orobanche spp.—seed germination is known to occur only in the presence of chemical stimulants released from plant roots. The recent
finding that these same chemicals promote the colonization of beneficial fungi has potentially important implications for
the control of parasitic plants. Far less is known about the early stages of parasitic plants that attach above-ground to
host shoots—e.g., Cuscuta spp. Seeds of these parasites lack germination stimulants, and it was only recently shown that foraging C. pentagona seedlings use airborne cues to locate and select among hosts. We review research on seed germination and host location by
the major parasitic weeds that attack agricultural crops, and discuss the implications of recent findings for the development
of sustainable and effective management strategies.
Parasitic Plants in Agriculture: Chemical
Ecology of Germination and Host-Plant
Location as Targets for Sustainable Control:
Justin B. Runyon, John F. Tooker, Mark C. Mescher
and Consuelo M. De Moraes
Abstract Parasitic plants are among the most problematic pests of agricultural
the close physiological connection between the established parasite and host plant
hindering efficient control using traditional methods. Seed germination and host
location are critical early-growth stages that occur prior to host attachment, and
provide promising targets for ecologically sound management of parasitic weeds.
Knowledge of parasite-host interactions, particularly chemical cues that induce par-
asite seed germination and mediate host location, should facilitate the development
of novel management approaches. In parasitic plants that attach to host roots—e.g.,
Striga and Orobanche spp.—seed germination is known to occur only in the pres-
ence of chemical stimulants released from plant roots. The recent finding that these
same chemicals promote the colonization of beneficial fungi has potentially impor-
tant implications for the control of parasitic plants. Far less is known about the early
stages of parasitic plants that attach above-ground to host shoots—e.g., Cuscuta
spp. Seeds of these parasites lack germination stimulants, and it was only recently
shown that foraging C. pentagona seedlings use airborne cues to locate and select
among hosts. We review research on seed germination and host location by the
major parasitic weeds that attack agricultural crops, and discuss the implications
of recent findings for the development of sustainable and effective management
Striga · Orobanche · Cuscuta · Strigolactones · Volatiles · Plant-plant
C.M. De Moraes (B)
Department of Entomology, Pennsylvania State University, 535 ASI building,
University Park, PA, 16802, USA
E. Lichtfouse (ed.), Organic Farming, Pest Control and Remediation
of Soil Pollutants, Sustainable Agriculture Reviews 1, DOI 10.1007/978-1-4020-9654-9 8,
C ?Springer Science+Business Media B.V. 2009
124J.B. Runyon et al.
2 The Major Parasitic Plants in Agriculture . . . . . . . . . . . . . . . . . . . .
3 Parasitic Plants Use Chemical Cues to Locate Hosts
3.1 Root Parasitic Plants: Germination Stimulants . . . . . . . . . . . . . . . .
3.2 Shoot Parasitic Plants: Plant Volatiles . . . . . . . . . . . . . . . . . . . .
4 Control Strategies Targeting Germination/Host Location
4.1 Suicidal Germination . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2 Inhibiting Germination of Parasitic Plants . . . . . . . . . . . . . . . . . .
4.3 Reducing the Production of Germination Stimulants
by Crop Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.4 Disruption of Volatile Host Location by Cuscuta spp. . . . . . . . . . . . . .
5 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . .
Approximately 4,500 species of flowering plants (more than 1% of all angiosperms)
are parasitic, obtaining some or all of their water and nutrients from other plants
(Kuijt, 1969; Nickrent, 2007). A small percentage of these parasitic species infest
agricultural crops and cause serious problems for farmers in many parts of the world
(Parker and Riches, 1993; Musselman et al., 2001). Few practical and economically
sound methods are available for controlling parasitic plant species (Gressel et al.,
2004; Rispail et al., 2007), in part because their physiological connection to host
plants limits the usefulness of most herbicides. Parasitic weeds can also be diffi-
cult to eradicate because they often produce large numbers of long-lived seeds. For
example, a single Orobanche sp. plant can produce over 200,000 dust-like seeds
that remain viable for 8–10 years (Parker and Riches, 1993). In addition, parasitic
plants that attack host roots can inflict serious damage to crop plants before the latter
emerge from the soil, making it difficult to diagnose infestations before economic
Breeding for host-plant resistance offers a potentially economical approach to
pea to Striga (Lane et al., 1993)—breeding programs have not provided effective
control and are challenging because plant resistance traits are often poorly charac-
terized, genetically complex, and of low heritability (Rispail et al., 2007). Genetic
engineering might help to overcome some of these difficulties (Bouwmeester et al.,
2003), but societal concerns about genetically modified technology may prevent
widespread adoption (Humphrey et al., 2006).
The search for improved or alternative approaches to controlling parasitic plants
in agriculture will be facilitated by an increased understanding of the complex
ecological and physiological interactions between parasitic plants and their hosts.
Parasitic Plants in Agriculture125
Host location is a critical part of the life cycle of the most damaging parasitic weeds,
which are obligate parasites that depend on the limited reserves available in seeds to
quickly locate suitable hosts. Host location thus seems a promising target for control
strategies. In this paper, we review the most important plant parasites of agricultural
crops, focusing on the chemical ecology of seed germination and host location, and
discuss the potential for manipulating these mechanisms to control these important
2 The Major Parasitic Plants in Agriculture
Parasitism originated independently several times during angiosperm evolution, and
the lifestyles of parasitic plants vary greatly across taxa (Kuijt, 1969; Nickrent et al.,
1998). Some species are facultative parasites that are able to survive in the absence
of hosts, while others are obligately parasitic and cannot develop independently. A
distinction can be drawn between hemiparasitic plants that possess chlorophyll and
are able to produce some of their required nutrients through photosynthesis and
holoparasitic plants that lack chlorophyll and are completely dependent on host
resources, but this distinction is not always clear-cut (Parker and Riches, 1993;
Press and Graves, 1995). A more definitive division can be drawn between para-
sitic plants that make below-ground attachments to host-plant roots and those that
attach above ground to host-plant shoots (Fig. 1). This review will focus on the most
economically important groups of plant parasites: witchweeds, Striga spp. (Scro-
phulariaceae); and broomrapes, Orobanche spp. (Orobanchaceae), which attach to
host roots; and dodders, Cuscuta spp. (Convolvulaceae), which make above-ground
attachments to host shoots (Parker, 1991).
Striga spp. (Fig. 2) are obligate root hemiparasites and infest an estimated two-
thirds of the cereals and legumes in sub-Saharan Africa, causing annual crop losses
estimated at US$7 billion annually, and negatively influencing the lives of more than
300 million people (Berner et al., 1995; Musselman et al., 2001). Several species of
but S. hermonthica and S. asiatica are the most widely distributed and destructive
(Oswald, 2005). Striga gesnerioides parasitizes broadleaf plants and is a serious
threat to cowpea production in many parts of Africa (Parker and Riches, 1993). In
the 1950s, S. asiatica was discovered parasitizing maize in the southeastern United
States, but its spread there has been halted by an intensive eradication program
Orobanche spp. (Figs. 1 and 3) are obligate root holoparasites that constrain
the production of many crops, primarily in the Mediterranean region, the Middle
East, and northern Africa (Parker and Riches, 1993). Among the six Orobanche
species considered serious pests, O. ramosa and O. aegyptiaca have the widest host
ranges and heavily damage a variety of crops, including tomato, potato, eggplant,
faba bean, lentil, peanut, chickpea, cucumber, cabbage, and sunflower (Parker and
Riches, 1993). Orobanche cumana has a host range limited to Asteraceae, and it
126J.B. Runyon et al.
hosts. Upon germination, the growth of Cuscuta seedlings is directed toward volatile compounds
released from nearby tomato plants (above-ground at left). The entire blend of tomato volatiles
(at least seven compounds) is most attractive, but three compounds from this blend individually
elicit directed growth of Cuscuta: (A) β-phellandrene, (B) β-myrcene, and (C) α-pinene (Runyon
et al., 2006). Seeds of the root parasites Striga and Orobanche will only germinate in response
to specific chemicals released by plant roots (below-ground at right). These germination stimu-
lants, called strigolactones, are active only within several millimeters of the host root. Orobanche
seedlings are shown with haustoria attaching to the tomato (inset, lower right). Strigol (D) was
the first germination stimulant identified. Strigol has not been isolated from tomato roots, but
similar strigolactones are produced. The chemical ecology of host location by parasitic weeds
provides early developmental points that could be exploited and manipulated for sustainable
Plant-derived chemical cues are used by both shoot and root parasitic weeds to locate
is an important pest of cultivated sunflowers (Parker and Riches, 1993; Press and
Graves, 1995). Infestation by Orobanche spp. can result in total crop loss (Bernhard
et al., 1998).
Cuscuta spp. have yellow-to-orange, rootless, leafless vines that attach to the
shoots of host plants (Fig. 4). They are obligate holoparasites, typically exhibit-
ing broad host ranges, and inflict serious damage to many crops, including forage
legumes (alfalfa, clover, lespedeza), potato, carrot, sugar beets, chickpea, onion,
cranberry, blueberry, and citrus (Dawson et al. 1994). Seeds of Cuscuta spp. have
been transported worldwide in contaminated shipments of crop plant seeds. Cus-
cuta pentagona is a major weed of tomatoes in California, causing yield losses of
Parasitic Plants in Agriculture127
Fig. 2 A sorghum field
infested with Striga
hermonthica (pink flowers) in
Ethiopia. Striga spp. attach to
host-plant roots and produce
green, flowering shoots that
emerge 1–2 months later.
Credit: Lytton J. Musselman
Fig. 3 Orobanche ramosa
parasitizing cabbage in
Sudan. Orobanche spp. attach
to host-plant roots, and their
flowering shoots, which lack
chlorophyll, emerge several
months later. Credit: Lytton J.
50–75% (Goldwasser et al., 2001). In China, several Cuscuta species inflict severe
damage on soybeans (Dawson et al., 1994).
3 Parasitic Plants Use Chemical Cues to Locate Hosts
The seeds of most parasitic plants contain a few energy reserves that allow lim-
ited growth. Consequently, seedlings can survive only a few days after germina-
tion before attaching to a host. The imperative of finding hosts quickly presumably
imposes strong evolutionary selection pressure favoring the development of efficient
128J.B. Runyon et al.
Fig. 4 Cuscuta pentagona
parasitizing tomato plants in
California. Cuscuta spp. lack
chlorophyll and attach
above-ground to host-plant
shoots. Credit: Jack Kelly
Clark, courtesy UC Statewide
host-location mechanisms. Both root and shoot parasitic plants utilize chemical cues
released by host plants for this purpose (Fig. 1).
3.1 Root Parasitic Plants: Germination Stimulants
Seeds of Striga and Orobanche spp. germinate only in the presence of chemical
compounds exuded from host roots (Fig. 1; Bouwmeester et al., 2007). Because
these germination stimulants, collectively called strigolactones, are unstable and
degrade rapidly in the soil, they occur at concentrations sufficient to induce ger-
mination only within a few millimeters of host roots (Fate et al., 1990). Concentra-
tion gradients of strigolactones may also facilitate directed growth of the parasite
radicle toward the host root (Dub´ e and Olivier, 2001). The sensitivity of parasite
seeds to these germination stimulants depends upon a conditioning period under
warm and humid conditions and concomitant synthesis of gibberellins in seed tis-
Parasitic Plants in Agriculture129
sues (Matusova et al., 2004). To date, several germination stimulants have been
isolated and identified from root exudates of both host and non-host plants. In work
with Striga lutea, the first germination stimulant (strigol) was isolated from the root
exudates of the non-host cotton (Cook et al., 1966). Strigol has since been found to
Additional strigolactone germination stimulants that have been identified include
sorgolactone from sorghum, orobanchol and alectrol from red clover, and 5-deoxy-
strigol from Lotus japonicus (Hauck et al., 1992; Yokota et al., 1998; Akiyama et al.,
2005). Recently, strigolactones have been shown to be apocarotenoids produced
by plants via the carotenoid pathway, rather than sesquiterpenoids as had previ-
ously been assumed (Matusova et al., 2005). The details of germination induction
by strigolactones are not understood (Bouwmeester et al., 2007), though possible
mechanisms have been proposed (Mangnus and Zwanenburg, 1992). Application
of ethylene can trigger seeds of Striga and Orobanche spp. to germinate, indicat-
ing that strigolactones may act by stimulating ethylene biosynthesis (Logan and
Stewart, 1991). The recent discovery that strigolactones serve as important cues for
plant-beneficial arbuscular mycorrhizal fungi (AMF; Akiyama et al., 2005; Besserer
et al., 2006) suggests that parasitic plants may have co-opted these signals to
recognize and locate host roots.
3.2 Shoot Parasitic Plants: Plant Volatiles
In contrast to root parasitic plants, germination of Cuscuta spp. seeds is not depen-
dent on stimulants derived from a host plant (Dawson et al., 1994). Instead,
seedlings must forage to locate potential hosts nearby. We recently reported that
seedlings of C. pentagona use host-plant volatiles to guide host location and selec-
tion (Fig. 1; Runyon et al., 2006). It had previously been suggested that Cuscuta spp.
seedlings forage randomly (Dawson et al., 1994), or orient their growth to various
light cues associated with the presence of host plants (Benvenuti et al., 2005). While
light cues may play a role in host location, we found that C. pentagona seedlings
exhibited directed growth toward tomato volatiles experimentally released in the
absence of any other plant-derived cues. Moreover, seedlings used volatile cues to
“choose” tomatoes, a preferred host, over nonhost wheat. Several individual com-
pounds from the tomato volatile blend were attractive to C. pentagona seedlings,
including α-pinene, β-myrcene, and β-phellandrene, while one compound from
the wheat blend, (Z)-3-hexenyl acetate, had a repellent effect. We subsequently
confirmed that C. pentagona seedlings respond to volatiles from a range of host
plants, including Impatiens, wheat (Runyon et al., 2006), and alfalfa (Mescher et al.,
2006). These findings provide a plausible mechanism to explain previous reports of
selective foraging by Cuscuta spp. (Kelly, 1990, 1992; Sanders et al., 1993; Koch
et al., 2004). It is tempting to speculate that the remarkably similar but unrelated
shoot-parasitic plants in the genus Cassytha (Lauraceae), and perhaps climbing
130 J.B. Runyon et al.
vines in general, might also use volatile cues to locate their hosts, but this possi-
bility has yet to be examined empirically.
4 Control Strategies Targeting Germination/Host Location
Considerable research has examined the possibility of exploiting germination
stimulants for control of Striga and Orobanche. Control strategies include: (1)
inducing “suicidal germination,” (2) inhibiting germination, and (3) reducing the
production of germination stimulants by crop plants. In addition, the newly dis-
covered role of strigolactones in the recruitment of symbiotic AMF (Akiyama
et al., 2005) has opened new possibilities for modifying the production of germina-
tion stimulants by host plants. We are not aware of any studies exploring the possi-
bility of disrupting host location by using Cuscuta spp., which have no germination
stimulants. However, the recently documented role of volatiles in host location by
C. pentagona, and the identification of several attractive and repellant compounds
(Runyon et al., 2006), suggests that such strategies might be plausible.
4.1 Suicidal Germination
Inducing the germination of Striga and Orobanche spp. seeds in the absence of a
suitable host plant results in “suicidal germination,” and subsequent reduction in
numbers of parasitic-plant seeds in soil. Both man-made and natural compounds
have been investigated for their ability to induce germination. Analogs of strigol
have been synthesized (e.g., GR 24 and Nijmegen 1) and are potent elicitors of ger-
mination in both Striga and Orobanche spp. (Wigchert et al., 1999); however, their
instability in soil (Barbiker et al., 1987), and the high cost of producing large quan-
tities of these compounds, have so far prohibited their use in agriculture (Humphrey
et al., 2006). Ethylene has been a valuable component of the eradication program
targeting Striga asiatica in the United States, where it induces about 90% germi-
nation when injected into the soil (Parker 1991). However, fumigating soil with
ethylene is likely to negatively influence AMF and other nontarget soil microorgan-
isms (Lendzemo et al., 2005). It has been proposed that ethylene-producing non-
pathogenic bacteria could be used to induce suicidal germination of Striga (Berner
et al., 1999), but a better understanding of bacteria/ethylene/crop interactions is
needed before this method can be used in agriculture. Other natural compounds,
including fungal toxins (Evidente et al., 2006) and methyl jasmonate (Yoneyama
et al., 1998) have been shown to induce germination of Striga and Orobanche spp.
seeds, but their potential uses in agriculture remain largely unexplored.
Planting nonhost trap crops that induce suicidal germination is perhaps the most
effective strategy currently available for Striga control (Oswald, 2005). Recent
studies in this area have focused on identifying and assessing the effectiveness of
potential trap crops (Gb` ehounou and Adango, 2003; Lins et al., 2006; Fen´ andez-
Aparicio et al., 2007; Khan et al., 2007) and the possibility of breeding for increased
Parasitic Plants in Agriculture131
production of germination stimulants (Botanga et al., 2003). Use of nitrogen-fixing
legumes as trap crops has the added benefit of increasing soil fertility, which can fur-
ther assist in Striga control because Striga thrive in poor soils (Parker and Riches,
1993). The efficacy of legume rotations could potentially even be improved by
inoculating crops with supplemental nitrogen-fixing rhizobia, in combination with
ethylene-producing bacteria, to simultaneously increase suicidal germination and
soil fertility (Ahonsi et al., 2003; Babalola et al., 2007).
Legumes have also proven useful as part of a novel “push-pull” (stimulo-
deterrent) pest management approach that illustrates the utility of increased plant
diversity, simultaneously reducing Striga and lepidopteran stemborer infestations
(Khan et al., 2000). Intercropping maize or sorghum with the leguminous trap
crop Desmodium spp. decreases parasitism by Striga spp. and repels oviposit-
ing stemborers, which subsequently move toward grasses bordering the field.
Desmodium suppress Striga, not only by producing a germination stimulant, but
also by producing chemicals that interfere with the development of haustoria
(Khan et al., 2002).
4.2 Inhibiting Germination of Parasitic Plants
The sensitivity of Orobanche spp. seeds to germination stimulants is positively cor-
related with the production of gibberellin during seed conditioning; therefore, their
germination can be inhibited by gibberellin biosynthesis inhibitors (Joel, 2000).
Applying the gibberellin inhibitor uniconazole to soil near sunflowers significantly
decreased broomrape parasitism and increased sunflower performance (Joel, 2000).
Sunflower varieties that are resistant to O. cernua exude coumarins that inhibit ger-
mination and are toxic to newly germinated seedlings (Serghini et al., 2001). More
of O. crenata and reduced parasitism when intercropped with legumes (Fen´ andez-
Aparicio et al., 2007). Seed germination can also be influenced by some amino
acids, which have been shown recently to have profound effects on the development
of O. ramosa. For instance, applying exogenous methionone almost completely
inhibited seed germination and reduced the number of developing Orobanche spp.
tubercles on tomato roots, possibly indicating that soil applications of amino acids
or amino acid-producing microbes might be used to manage parasitic weeds (Vurro
et al., 2006).
4.3 Reducing the Production of Germination Stimulants
by Crop Plants
Decreased production of germination stimulants is the best characterized
mechanism of crop resistance to parasitic plants (Rispail et al., 2007). This strategy
has been exploited successfully in sorghum breeding to confer resistance of cer-
tain sorghum varieties to Striga (Haussmann et al., 2000). Resistance is apparently
132 J.B. Runyon et al.
absent in some crop plants, including cowpea and maize (Rubiales, 2003), although
considerable variation has been reported among genotypes of tomato and Arabidop-
sis (Goldwasser and Yoder, 2001; El-Halmouch et al., 2006). Recent findings sug-
gest that selecting for reduced production of germination stimulants might neg-
atively influence crop interactions with beneficial AMF (Akiyama et al., 2005).
Recognition that strigolactones that induce parasitic plant seeds to germinate also
recruit nutrient-supplying AMF suggests that manipulating mycorrhizal coloniza-
tion could be used to manage parasitic plants (Akiyama et al., 2005). Recent reports
show that nutrient deficiency, which in some cases is mitigated by AMF, can
increase strigolactone production by potential host plants (Yoneyama et al., 2007).
Moreover, colonization of host plants by AMF can down-regulate the production
of germination stimulants (Lendzemo et al., 2007; Bouwmeester et al., 2007), sug-
gesting that enhancing AMF colonization of crop seedlings in fields could reduce
strigolactone production, and possibly reduce the numbers of parasitic plant seeds
4.4 Disruption of Volatile Host Location by Cuscuta spp.
The discovery that Cuscuta spp., like root-parasitic plants, use chemical cues to find
hosts, may lead to control strategies aimed at disrupting host location analogous to
those described for root-parasitic plants. Plant volatiles, even more so than strigolac-
tones,aresensitivetoenvironmental variables (DeMoraesetal.,1998,2001;Tooker
and De Moraes, 2007; Tooker et al., 2008) and could potentially be manipulated
(cf. Turlings and Ton, 2006) to reduce the attraction of Cuscuta spp. seedlings. In
addition, the production of plant volatiles is a heritable trait (Degen et al., 2004) that
could potentially be incorporated into a plant-breeding program for Cuscuta resis-
tance. Moreover, because at least one repellent compound ([Z]-3-hexenyl acetate)
has been identified, a “push-pull” approach for control of Cuscuta spp. can be envi-
sioned similar to that used for African stemborers. However, little to no work to
date has examined the feasibility of such approaches, and further work is needed to
elucidate how Cuscuta spp. perceive and respond to plant volatiles.
In spite of intensive research, adequate strategies for controlling parasitic plants
remain elusive, and these weeds continue to threaten agricultural crops worldwide.
Chemically mediated interactions between early-stage parasitic plants and their
hosts play a key role in infestation and may be exploited for control. Recent
advances in this area suggest a number of potentially fruitful approaches, including
the prospect of simultaneously managing beneficial symbionts and parasitic weeds.
For example, implementing cultural practices that favor AMF, such as reducing
tillage and fungicide application, could improve growth and increase drought tol-
erance in crops (Plenchette et al., 2005), and potentially reduce Striga infestations
Parasitic Plants in Agriculture133
(Lendzemo et al., 2007). Additional research is needed to understand the mech-
anisms underlying strigolactone perception and responses in both parasitic plants
and AMF. Intercropping with nonhost plants that induce “suicidal germination”
and/or are allelopathic to root parasites (e.g., Khan et al., 2002) is another promis-
ing approach that warrants continued efforts to identify potential trap crops and
improve their efficacy. Recent work on the role of volatiles in host location by
C. pentagona suggests that control strategies aimed at disrupting host location might
be used against parasites that make above-ground attachments, but more work is
needed in this area. It seems unlikely that any single method alone will provide
long-term control of parasitic weeds. An integrative approach incorporating one or
several methods targeting the chemistry used in host location by parasitic weeds is
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