Available online at www.sciencedirect.
com
Host plant resistance to parasitic weeds; recent progress and
bottlenecks
John I Yoder1 and Julie D Scholes2
Parasitic witchweeds (Striga spp.) and broomrapes
(Orobanche and Phelipanche spp.) directly invade the roots of
crop plants connecting to the vascular system and abstracting
nutrients and water. As a consequence they cause devastating
losses in crop yield. Genetic resistance to parasitic weeds is a
highly desirable component of any control strategy. Resistance
to parasitic plants can occur at different stages of the parasite
lifecycle: before attachment to the host, during penetration of
the root or after establishment of vascular connections. New
studies are beginning to shed light on the molecular
mechanisms and signaling pathways involved in plant–plant
resistance. The first resistance gene to Striga, encoding a CC-
NBS-LRR Resistance protein (R) has been identified and
cloned suggesting that host plants resist attack from parasitic
plants using similar surveillance mechanisms as those used
against fungal and bacterial pathogens. It is becoming clear
that the salicylic acid (SA) signaling pathway plays an important
role in resistance to parasitic plants and genes encoding
pathogenesis-related (PR) proteins are upregulated in a
number of the resistant interactions. New strategies for
engineering resistance to parasitic plants are also being
explored, including the expression of parasite-specific toxins in
host roots and RNAi to silence parasite genes crucial for
development.
Addresses
1
Department of Plant Sciences, University of California-Davis, Davis,
CA 95616, USA
2 recent progress in these areas [12–15].
Department of Animal and Plant Sciences, University of Sheffield,
Sheffield S10 2TN, UK
Corresponding authors: Yoder, John I (jiyoder@ucdavis.edu)
Current Opinion in Plant Biology 2010, 13:478–484
This review comes from a themed issue on
Biotic interactions
Edited by Jane E. Parker and Jeffrey G. Ellis
Available online 2nd June 2010
1369-5266/$ – see front matter
# 2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2010.04.011
Introduction
Parasitism has originated at least a dozen times during
angiosperm evolution resulting in a diversity of parasitic
plant forms and habits [1,2]. Parasitic plants directly
invade other plants via parasite encoded haustoria in
order to rob them of water and nutrients. The effects
on the host plant can be debilitating and some of the
Current Opinion in Plant Biology 2010, 13:478–484
world’s most devastating agricultural pests are parasitic
weeds. The most notorious — Striga, Orobanche, and
Phelipanche (formerly within Orobanche [3]), are in the
Orobanchaceae, a family of about 30 parasitic plant gen-
era that invade hosts via their roots [4,5]. Striga, or witch-
weed, is particularly problematic. In sub-Saharan Africa
up to 60% of the arable farmland under cultivation with
cereals and grain legumes are infested with one or more
Striga species. While yield losses are generally difficult to
quantify, farm losses from Striga infestations are esti-
mated to negatively impact the food supply of over 100
million people [6–9]. And importantly, the impact of
parasitic weeds on international agriculture is ever-
increasing [10].
The field control of parasitic weeds is challenging
because the host and pathogen are both plants, their
lifecycles are highly coordinated, the pathogenesis occurs
underground, and the countries in which the weeds are
most abundant are often impoverished [11]. Over the past
several decades extensive research has been aimed at
practical, low-cost methods for limiting Striga and Oro-
banche in the field. These approaches have been augmen-
ted by breeding programs directed toward introgressing
natural resistance mechanisms into field crops. The
reader is directed toward several excellent reviews for
Host resistance is generally considered a key component
of integrated pest management. Host resistance to para-
sitic plants is a multi-component process that can occur at
different stages of the parasite lifecycle [16]. For the
purpose of this review these stages will be combined
into three general periods: preattachment, parasite estab-
lishment, and postestablishment maturation. This review
focuses on recent progress in our understanding of the
molecular and genetic mechanisms acting at each stage
with a particular focus on the relevance of these stages to
developing parasite-resistant crops.
Host resistances functioning before parasite
attachment
Parasitic weeds use host-encoded molecules to trigger
different stages of parasite development. Because host
factors are critical for parasite success, they are obvious
targets for resistance. Two stages in early parasite
development are regulated by known molecules: seed
germination and haustorium development. Mutations in
host plant genes that encode the biosynthesis or release of
signaling molecules can reduce parasite viability.
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 Host plant resistance to parasitic weeds Yoder and Scholes 479

Host germination stimulants Low germination stimulant genotypes of sorghum have

Striga and Orobanche seeds require exposure to specific
terpene lactones, collectively called strigolactones, to
germinate [17]. Strigolactones had been characterized
as Striga germination factors for over 25 years before
seemingly unrelated grafting experiments of stem
branching mutants identified strigolactones as a new class
of plant hormones [18,19,20]. Strigolactones are syn-
thesized in plant roots and translocated to above ground
parts where they act as inhibitors of stem branching [21].
Strigolactones have a common four ringed structure com-
prising a tricyclic lactone (ABC ring) and a butyrolactone
(D ring) with the CD ring moiety being critical for
germinating activity [22] (Figure 1). Striga and Orobanche
have exploited the release of these natural hormones into
the rhizosphere as chemical cues of a neighboring host
root [23].
enhanced resistance to Striga because of the reduction in
Striga germination [24]. Low germination stimulation was
also implicated in some legume and sunflower accessions
that showed enhanced resistance to Orobanche species
[25]. While the structural chemistry of strigolactones is
known, the mechanisms underlying low germination
stimulant phenotypes (e.g. alterations in the biosynthesis,
regulation, degradation, or exudation of stimulants) are
not.
Strigolactones are formed following oxidative cleavage of
unknown carotenoid substrates by carotenoid cleavage
dioxygenase enzymes (CCD). Roots from pea or rice ccd7
and ccd8 mutants have decreased levels of strigolactones,
induce less AM fungal hyphae branching, and are less
effective at germinating Orobanche and Striga seeds

Figure 1

Host molecules needed by the parasite. The derivation of three host molecules used as developmental signals by parasitic plants. Strigolactone is a
Striga germination stimulant produced by the carotenoid pathway. The flavonoid molecule peonidin and dimethoxybenzoquinone are both haustorial
inducing factors. DMBQ is produced through the action of laccases and peroxidases acting on lignin components [62].

www.sciencedirect.com Current Opinion in Plant Biology 2010, 13:478–484

480 Biotic interactions

[19,20]. Reduction of CCD7 transcripts in tomato by
antisense RNA resulted in plants with decreased levels of
strigolactones and reduced Orobanche germination [26].
Strigolactones also affect above ground plant form and
hyphae branching of arbuscular mycorrhizal fungi [27], so
strigolactone mutants, while reduced in parasitic weed
germination, may negativity impact plant productivity
and rhizosphere composition. Potential applications of
strigolactones in parasitic weed control have been more
fully discussed elsewhere [28].
resistance was accompanied by the accumulation of
unknown substances at the endodermal barrier, although
this is not always the case. In the rice cultivar Nipponbare,
which exhibits strong resistance to some ecotypes of S.
hermonthica, the parasite invades the cortex but the para-
site radical grows around the vascular cylinder suggestive
of a lesion in the signaling pathway(s) involved in pene-
trating between endodermal cells [35] (Figure 2). This
phenotype has subsequently been observed at different
frequencies in other rice cultivars [36].

Haustorium inducing factors

Haustoria are the invasive structures that develop at the Figure 2

tips of Striga radicals in response to host root contact.

Certain phenolics, flavonoids, and quinines have been
identified that induce haustorium development when
added to parasite radicals in vitro [29]. While most of
these are phytochemicals, the only haustorium inducing
factor isolated directly from host roots is 2,4-dimethoxy-p-
benzoquinone (DMBQ) [30]. DMBQ is widespread in
plants and is generated through the oxidative degradation
of lignin and decarboxylation of phenolic acids (Figure 1).
DMBQ is released from host cell walls by peroxidases
which are activated by hydrogen peroxide generated by
the Striga radical. Striga thereby elicits the host to produce
a signal necessary for parasite development in a process
termed semagenesis [31].

Some host genotypes, particularly wild relatives of sor-

ghum [32] and maize, for example, Tripsacum dactyloides (a
wild relative of maize), have a reduced ability to initiate
haustoria. In the latter case this is likely to be due to the
exudation of low amounts of haustorial inducing factor as
the addition of syringic acid increased the number of
radicals forming haustoria [33]. In other cases low haus-
torial initiation may be due to the production of inhibitors
but this is a little researched area at present [32].

Host resistance to parasite establishment

Successful penetration of the root cell layers and estab-
lishment of host–parasite vascular continuity are essential
for the survival of Orobanche and Striga and there are
examples of host resistances that block parasite devel-
opment in the cortex, at the endodermis, and before or
after connection to the vascular system. Resistance that
occurs in the cortex is often associated with the deposition
of compounds such as callose (e.g. Pisum sativum and Vicia
sativa infected with O. crenata) and suberin (e.g.
Helianthus annus infected with O. cumana) and is associ-
ated with protein crosslinking in the host cell walls and
the accumulation of phenolic compounds [25]. The endo-
dermis, often considered to be a major barrier to parasite
infection, is the site of resistance expression in a number
of host–parasite associations including sorghum to S.
asiatica, a maize inbred line derived from Zea diploperennis
(a wild relative of maize) to S. hermonthica [34] and sun-
flower and vetch to O. cumana [25]. In these examples
Host resistance to parasite establishment. Transverse sections of
embedded tissue of susceptible (Kasalath) and resistant (Nipponbare)
rice roots 3, and 21 days after inoculation with Striga hermonthica. In the
susceptible interaction the parasite penetrates the cortex and
endodermis and connects to the xylem vessels of the host allowing the
haustorium to differentiate. In contrast, in the resistant interaction,
although the parasite penetrates the cortex, it is unable to breach the
endodermal barrier and grows around the host vascular cylinder. The
parasite is unable to access host water and nutrients and the haustorium
does not differentiate and the parasite dies. The scale bar represents
0.1 mm. En, endophyte (internal part of haustorium); Hc, host root
cortex; He, host endodermis; Hx, host xylem; Hx–Px, host–parasite
xylem continuity; Hy, hyaline body; P, parasite haustorium; and Px,
parasite xylem vessels. Adapted from Gurney et al. [35].

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Knowledge of the molecular basis underlying resistance
phenotypes is essential for crop improvement and the
development of novel control strategies. Recently the
first resistance gene to Striga was identified and cloned
[37]. S. gesnerioides exhibits a clear race structure; at least
seven races of this parasite have been identified based on
genetic diversity analysis and on their differential reac-
tion to a panel of cowpea cultivars [38], suggesting a gene-
for-gene interaction in the cowpea–S. gesnerioides host–
parasite association. The resistance response of cowpea
cultivar B301 to race 3 (SG3) of S. gesnerioides is charac-
terized by an inability of the parasite to penetrate the
endodermis and necrosis of host tissue at the point of
attachment. A simple sequence repeat (SSR) was ident-
ified in all cultivars of cowpea resistant to S. gesnerioides
SG3 which was not associated with resistance to any other
races. This allowed the full-length gene to be cloned and
sequenced. The sequence predicted a CC-NBS-LRR R
protein (named RSG3-301). When RSG3-301 was silenced
in the resistant cultivar B301 (using virus-induced gene
silencing (VIGS)) compatibility to S. gesnerioides race 3
was restored but the cultivar remained resistant to other
races of the parasite (SG2 and SG5) supporting the
hypothesis of a gene-for-gene interaction. R genes recog-
nize, directly or indirectly, pathogen effectors (often
termed Avr genes) to trigger plant defence responses.
As yet parasitic plant effectors have not been identified.
However, the imminent release of genome sequence
databases for the angiosperm parasites S. hermonthica,
P. aegyptiaca and Triphysaria versicolor (www://
ppgp.huck.psu.edu/) coupled with advances in functional
analysis of effector proteins makes this an exciting area for
future investigation.
While most resistance to Striga and Orobanche species is
considered to be quantitative (i.e. governed by multiple
genes) O. cumana also exhibits a clear race structure (five
races A–E have been identified) with respect to sunflower
cultivars, suggesting the existence of race-specific resist-
ance [39]. In this system the corresponding resistance
genes which are monogenically and dominantly inherited
have been termed Or1–Or5 but await identification at the
sequence and protein level. The identification of major
genes for resistance and their location on the host genome
will aid the pyramiding of multiple R genes in cultivars,
prolonging the effectiveness of this major gene resistance.
Recent studies on profiling changes in gene expression
during parasitic plant–host resistance interactions are also
beginning to shed light on the molecular basis of some of
the downstream signaling pathways and induced
defences involved [38,40,41,42]. In many of the resist-
ance responses to parasitic plants described above, para-
site death is associated with host necrosis at the point of
parasite attachment although whether this represents a
hypersensitive response (HR) is controversial. Certainly,
in the rice cultivar Nipponbare expressing resistance to S.
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Host plant resistance to parasitic weeds Yoder and Scholes 481
hermonthica, genes encoding homologs of hypersensitive
response proteins were upregulated [41]. It is becoming
increasingly clear that the salicylic acid (SA) and to some
extent the jasmonic acid (JA) signaling pathways play
important roles in resistance to parasitic plants. The SA
pathway is often activated in response to biotrophic
fungal pathogens leading to the expression of suites of
PR genes whereas the JA pathway is often important in
resistance to necrotrophic pathogens and insect pests,
although it is clear that the SA and JA defence pathways
can interact either antagonistically or synergistically [43].
In a cowpea accession, IT97K-499-35, which exhibits race-
specific resistance to race SG3 of S. gesnerioides PR-5 tran-
script levels were dramatically elevated when compared to
those of a susceptible interaction, a nonhost interaction or to
uninfected roots [38]. Several SA-induced PR gene tran-
scripts or proteins were elevated in the resistance response
of sunflower to O. cumana [42], Arabidopsis to O. ramosa [44]
and sorghum [45] and rice [41] to S. hermonthica. In the
latter study an analysis of changes in gene expression, using
rice microarrays, revealed upregulation of transcripts
encoding endochitinases (PR-3), glucanases (PR-2), and
thaumatin-like proteins (PR-5). Members of the WRKY
family of transcription factors, which are involved in reg-
ulating defence pathways were also upregulated. These
included OsWRKY45, OsWRKY62, and OsWRKY76
which were also induced in rice leaves resistant to M. grisea
and OsWRKY45 and OsWRKY62 which were upregulated
in rice tissue treated with SA [46]. A number of studies have
evaluated the effectiveness of applications of SA to Oro-
banche spp. SA consistently promoted resistance, in the case
of clover roots infected with O. minor, by the activation of
defence responses leading to lignification of the endoder-
mis [47]. To date SA inducing chemicals have not been
applied to field grown crops to test their effectiveness as
part of a control strategy.
The induction of genes involved in JA biosynthesis has
been observed in compatible interactions between Oro-
banche species and their hosts [40] but the involvement of
JA in resistance is less clear. In a recent study of resistance
in tomato to the shoot parasite Cuscuta pentagona a role for
both JA and SA was proposed [48]. In this study tomato
shoots were initially challenged with C. pentagona when 10
days old resulting in a compatible interaction. However, a
second challenge when tomato plants were 20 days old
resulted in a hypersensitive-like resistance response which
was accompanied by a sequential increase in JA followed
by SA, perhaps suggesting that coordinated synthesis of
these hormones was required for effective resistance.
Host resistances acting after parasite
establishment
Resistance can occur following successful connection of
parasites to the host vascular system. In some pea geno-
types that are resistant to O. crenata the host vascular cells
Current Opinion in Plant Biology 2010, 13:478–484
482 Biotic interactions
fill with mucilage-like compounds that block the trans-
port of nutrients to the parasite leading to gradual brown-
ing and death of tubercles [49]. In other resistant
interactions, for example, T. dactyloides infected with S.
hermonthica [33], the parasite makes connections to the
host xylem and, although there is no blockage of the
vessels, the parasite dies. S. hermonthica individuals
attached to susceptible maize roots were manipulated
so that secondary haustoria were attached to the roots
of T. dactyloides, thus bridging the two hosts. The sec-
ondary haustoria on T. dactyloides failed to differentiate
properly and subsequent secondary haustoria formation
on the susceptible maize host was also impaired,
suggesting that the inhibitory compound(s) was(were)
mobile within the parasite haustorial root system. These
results can be interpreted as some type of toxin being
translocated from the host into the parasite.
Expressing a pest-specific toxic protein in a host plant is a
proven strategy for controlling herbivorous pests [50].
Expression of the antimicrobial toxin sarcotoxin IA gene,
originally from the flesh fly Sarcophaga pregrin, in tomato
roots resulted in a 50% reduction in the number of
emerging O. aegyptiaca [51,52]. The authors reported a
3–5 times increase in fruit yield when the transgenic
plants were grown under Orobanche pressure [51]. The
mechanism by which sarcotoxin is preferentially toxic to
Orobanche but not Solanaceae is unclear. A defensin gene
encoding a protein expressed in roots of broomrape-
resistant sunflower is upregulated by Orobanche exposure
[53]. The protein was expressed in E. coli and was toxic
when applied to radicals of Orobanche but not Striga nor
Arabidopsis [53]. Mobilization of such defensins could
provide a parasite-specific toxin if they are mobilized
across the haustorium.
A promising, often discussed strategy employs interfering
RNA (RNAi) as the parasite-specific toxin. The general
approach is to transform a host plant with a double stranded
RNAi construction specifically targeted against a gene
critical for parasite development. If the hairpin is designed
from sequences specific for the parasite, no phenotype is
expected in the host even when the double stranded RNA
is processed into small interfering, siRNAs [54,55]. How-
ever, translocation of the RNAi silencing signal across the
haustorium and into the parasite should inhibit parasite
gene expression and subsequently survivability. This gen-
eral strategy has been employed to generate novel resist-
ances against parasitic nematodes [56,57].
The potential to regulate the expression of genes in a
parasite by providing a host transgenic for RNAi was
demonstrated by silencing of the marker beta-glucuroni-
dase (GUS) gene in transgenic roots of the hemiparasite
Triphysaria versicolor [58]. When the GUS expressing
parasite root was allowed to parasitize lettuce or Arabidopsis
bearing a hairpin GUS construction, there was reduction in
Current Opinion in Plant Biology 2010, 13:478–484
GUS transcript and enzyme levels at and several cm from
the haustorial junction. The silencing signals moved bidir-
ectionally across the haustorium as observed by GUS
silencing in a transgenic Arabidopsis parasitized by a single
Triphysaria that also parasitized an RNAi plant. There has
been one report of reduced Orobanche viability by RNAi
silencing [59]. Tomato plants were transformed with a
hairpin RNAi targeted toward the Mannose 6-Phosphate
Reductase (M6PR) gene of Orobanche aegyptiaca. The
M6PR protein is required for the biosynthesis of mannitol
which is thought to be used by parasitic plants to establish
the osmotic drive of host solute into the parasite [60]. When
Orobanche was infected onto transgenic roots, there was a
significant reduction in M6PR mRNA and the total amount
of mannitol in the Orobanche. Intriguingly, the authors
reported an increase in Orobanche mortality up to 20 times
higher on transgenic than nontransgenic lines [59]. It will
be interesting to see how this system holds up in the field. A
similar RNAi strategy was not successful at preventing
Striga infection of maize [61]. This group targeted five S.
asiatica genes: two required for fatty acid biosynthesis, one
for the synthesis of aromatic amino acids, one for the
biosynthesis of adenosine monophosphate, and a fifth gene
controlling vacuole morphogenesis. Though there were
some differences in S. asiatica growth in different trans-
genic maize, none of the 11 transgenic maize lines tested at
the time of publication were resistant [61].
Conclusions
Similar to other agricultural pests, the control of parasitic
weeds will require the integration of effective, sustain-
able cultural practices with the planting of genetically
optimized seed. Development of novel, robust host resist-
ances will require a better understanding of the molecular
basis underlying parasitic plant specific processes. Knowl-
edge about the processes employed by parasitic plants has
lagged behind that of microbial plant pathogens, but with
the increasing availability of parasite genomic resources it
should be possible to determine which of the microbial
resistance mechanisms are also effective against parasitic
plants.
A general conclusion emerging from recent work is that
parasitic plants seem to adapt processes and mechanisms
common to all plants for parasitic purposes. Examples
include the use of strigolactone hormones as germination
stimulants and the engagement of canonical resistance
genes for parasitic plant defense. A deeper understanding
of the genetic differences between parasitic weeds and
autotrophic plants should drive increased interests in the
biology and control of parasitic weeds. Certainly the need
is there.
Acknowledgements
Work in the Yoder lab is supported by a grant from the National Science
Foundation # 0236545. Work in the Scholes lab is supported by grants from
the Biotechnology and Biological Sciences Research Council (BBSRC), UK.
www.sciencedirect.com

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