Review TRENDS in Plant Science Vol.12 No.
Rhizosphere communication of plants,
parasitic plants and AM fungi
Harro J. Bouwmeester1,2, Christophe Roux3, Juan Antonio Lopez-Raez2
and Guillaume Becard3
1
Laboratory for Plant Physiology, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
2
Plant Research International, PO Box 16, 6700 AA Wageningen, The Netherlands
3
Laboratory for Cell Surfaces and Signalling in Plants, UMR 5546 Toulouse 3 University-CNRS, Castanet-Tolosan, France
Plants use an array of secondary metabolites to defend
themselves against harmful organisms and to attract
others that are beneficial. However, the attraction of
beneficial organisms could also lead to abuse by mal-
evolent organisms. An exciting example of such abuse is
the relationship between plants, beneficial mutualistic
arbuscular mycorrhizal fungi and harmful parasitic
plants. Signalling molecules called strigolactones, which
are secreted by plant roots in low concentrations, induce
the growth of both obligate biotrophs. Here, we review
the importance of strigolactones for these two inter-
actions and discuss possible developments that should
further clarify the role of these signalling molecules in
rhizosphere processes.
Communication of plants with other organisms
Plants produce a large variety of chemicals, usually called
secondary metabolites because of their presumed second-
ary role in plant growth and survival, with a wide range of
chemical structures [1]. Many of these secondary metab-
olites have been shown to be of ecological significance
because, for example, they are toxic to insects and plant
pathogens [13], or because they act as signalling mol-
ecules, in the air as well as in the rhizosphere [4,5]. For
example, the colonization of legume roots by nitrogen-
fixing bacteria, which is facilitated by host-root-secreted
flavonoids, and the attraction of natural enemies of herbi-
vorous insects by host-plant-produced volatiles [69]. The
evolution of a signalling relationship between mutually
beneficial organisms is a process driven by both partners,
but these sophisticated symbiotic relationships create an
opportunity for malevolent organisms to eavesdrop [10].
An amazing example of the evolution of a highly sophis-
ticated signalling relationship between two symbiotic
organisms that is abused by a third organism is the
relationship between plants, arbuscular mycorrhizal
(AM) fungi and parasitic plants (Figure 1).
Parasitic plants
Approximately 1% of the angiosperm plant species
have evolved the ability to parasitize other plants [5,11,
12]. The degree of specialization in parasitism varies from
Corresponding authors: Bouwmeester, H.J. (harro.bouwmeester@wur.nl);
Becard, G. (guillaume.becard@scsv.ups-tlse.fr).
Available online 9 April 2007.
www.sciencedirect.com 1360-1385/$ see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2007.03.009
facultative parasites, such as Rhinanthus spp. to obligate
parasites such as Striga spp. (whitchweeds) and Oro-
banche spp. (broomrapes) that can only survive if they
grow on the roots of a host plant [1114]. These root
parasites attach themselves to the roots of their hosts
using a specialized organ called a haustorium; they use
this organ to obtain water, assimilates and nutrients from
the host [5,15]. Although many Striga and Orobanche
species are components of natural vegetations and are
appreciated for their colourful flowers, these parasitic
plants are particularly known because they can be a nui-
sance in agriculture, where they can completely destroy
harvests. Striga spp. are mainly found in Africa, particu-
larly in West Africa where >60% of the cereal growing
areas are infested [16]. Orobanche spp. parasitize crops
such as legumes, crucifers, tomato and sunflower in the
more temperate regions around the globe [17,18]. The
seeds of parasitic plants are tiny after germination they
must attach to a host root within days or they will die. To
prevent the seeds from germinating too far from a host
root, parasitic plants have evolved a requirement for
so-called germination stimulants, compounds that are
produced by the roots of their hosts [10,19] (Figure 1).
Compounds from several different secondary metabolite
classes have been described to have germination stimulant
activity: sorgoleone, an isoflavanone, sesquiterpene lac-
tones and strigolactones [1923]. Strigolactones have been
detected in low quantities (cotton seedlings secreted
15 pg of strigol/day [24]) in the exudates of a range of
plant species, such as maize (Zea mays), sorghum (Sor-
ghum bicolor), pearl millet (Pennisetum glaucum), cotton
(Gossypium hirsutum), red clover (Trifolium pretense),
tomato (Solanum lycopersicon), Lotus japonicus and
Menispermum dauricum (Figure 2) [2528]. Usually, exu-
dates contain more than one strigolactone and differences
in the composition exist even between varieties of one
species [25]. Given the presence of strigolactones in the
root exudates of many monocot and dicot species, it
appears that the strigolactones occur throughout the plant
kingdom and play an essential role in plant biology [29].
Strigolactones are also important as root-recognition
signals for AM-fungi
The strigolactone 5-deoxystrigol was recently identified as
the factor in root exudates of L. japonicus that is responsible
 Review TRENDS in Plant Science Vol.12 No.5 225

Figure 1. Underground communication between plants, arbuscular mycorrhizal (AM) fungi and parasitic plants. Plants produce and release secondary metabolites into the
rhizosphere to establish communication with other organisms. Strigolactones are an important class of signalling molecules. They were previously isolated as seed-
germination stimulants for parasitic plants [19] but later shown to also induce hyphal branching in AM fungi [30,35]. Indirect communication between AM fungi and
parasitic plants as evident from reduced Striga infection when plants are colonized by AM fungi [52] seems to be mediated through the strigolactones as well.

for inducing hyphal branching in germinating mycorrhizal
spores (Figures 1 and 2) [30]. In the arbuscular mycorrhizal
symbiosis, plants obtain water and mineral nutrients from
their fungal partners, enabling them to survive under var-
ious stressful conditions [3133]. AM fungi are obligate
symbionts and depend on the carbon provided by their plant
host to complete their developmental cycle. In the presence
of a growing root, the germ tubes ramify intensively and the
fungus fully engages its catabolic metabolism [34]. This pre-
symbiotic invasive growth facilitates root contact, penetra-
tion and colonization. Other strigolactones such as strigol,
sorgolactone, and the synthetic analogue GR24 have also
been shown to have the same activity as 5-deoxystrigol [30]
(Figure 2). Sorgolactone is extremely active it has been
shown to induce branching at a concentration as low as
10 13 M [35].
Molecular data and studies of fossils suggest that AM
fungi have facilitated the adaptation and evolution of
primitive plant species to life on land, and after more than
400 million years of co-evolution, plants and AM fungi have
become highly interdependent [32,3638]. Today AM fungi
colonize roots of the vast majority of land plant species,
with the exception of members of the Brassicaceae, Car-
yophyllaceae, Amaranthaceae (Chenopodiaceae) and Urti-
caceae [39]. The mycorrhizal symbiosis probably depends
on a subtle and constant molecular dialogue between the
two partners, of which host recognition is a first important
step. Recent experimental data show that strigolactones
are directly responsible for mycorrhizal establishment
[40]. Apparently, during the co-evolution of the two
partners, strigolactones were selected to facilitate this
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process of host recognition. Mycorrhizal symbiosis,
therefore, led to the prevalence of strigolactones through-
out the plant kingdom and then, indirectly, enabled the
later evolution of the host detection mechanism of parasitic
plants using the same compounds.
Effects of environmental factors on exudation of
signalling molecules
One of the primary roles of AM fungi in the symbiotic
relationship with plants is the delivery of mineral nutri-
ents, particularly, phosphate [31,32]. In many areas of the
world, the concentration or availability of this essential
mineral nutrient in the soil is limited and this has a
significant impact on plant growth and health. AM fungi
can help to improve the uptake of phosphate and hence
improve plant growth in these areas [41,42]. In agreement
with the important role of AM fungi in the acquisition of
phosphate, it has been shown that root exudates produced
by plants grown under phosphate limitation are more
stimulatory to AM fungi than exudates produced under
adequate phosphate nutrition [43,44]. It has been reported
in the literature that phosphate starvation results in
increased exudation of several compounds. These include
not only metabolites to enhance the availability of phos-
phate such as citrate, but also compound classes such as
isoflavonoids and phenolics [4446]. Interestingly, the
exudation of the strigolactone orobanchol by red clover
roots is also stimulated under low phosphate conditions
[47,48]. Furthermore, in tomato, root exudates of plants
grown under phosphate starvation induced more hyphal
branching of germinating spores of Gigaspora rosea and at
226 Review TRENDS in Plant Science Vol.12 No.5

Figure 2. Biosynthesis of carotenoid-derived (signalling) molecules in plants. Solid arrows represent enzymatic steps. Names of enzymes are shown in red; names of
intermediates are shown in black. Strigolactones are depicted in blue. Enzymes: CCD, carotenoid cleavage dioxygenase; GGDP synthase, geranylgeranyl diphosphate
synthase; NCED, 9-cis-epoxycarotenoid dioxygenase. Intermediates: DMADP, dimethylallyl diphosphate; GGDP, geranylgeranyl diphosphate; IDP, isopentenyl
diphosphate.

the same time induced a greater proportion of the seeds
of the parasitic plant Orobanche ramosa to germinate
(J.A. Lopez-Raez, H.J. Bouwmeester, V. Gomez-Roldan
et al., unpublished). We have shown that this is also true
for hosts of Striga spp. (Z. Sun, G. Becard and H.J. Bouw-
meester, unpublished). This effect could explain the
dramatic extent of the Striga problem in areas with limited
phosphate availability [47] and the suppressive effect of
phosphate fertilization on Orobanche minor [49].
Several groups have reported that colonization by AM
fungi can reduce the infection of crops such as sorghum and
maize by Striga [50,51] (Figure 1). Germination bioassays
on exudates of mycorrhizal and control plants suggest
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that this is, at least partly, caused by a down-regulation
of strigolactone formation after mycorrhizal colonization
(Z. Sun, M.H. Walter, H.J. Bouwmeester et al., unpub-
lished) [52]. This suggests that the process of mycorrhizal
auto-regulation reported by Vierheilig and co-workers
could at least partly be mediated through the
production of strigolactones [53]. The effects of phosphate
and AM-fungi on the production of signalling molecules by
plants could be an interesting explanation for the tran-
sition of Striga spp. from being relatively innocent com-
ponents of African grasslands, where they co-exist with
their hosts at relatively low infection levels, to a more
serious biological constraint in cereal crops where the
 Review TRENDS in Plant Science
infection level is much higher. The existence of AM fungal
hyphal networks and/or the likely better phosphate avail-
ability in the natural ecosystem could keep strigolactone
exudation by the grassland species within limits that do
not induce large numbers of Striga seeds to germinate and
infect their hosts.
Perception and mechanism of action of
strigolactones
The mechanisms by which strigolactones induce seed
germination of parasitic plants and hyphal branching of
AM fungi are poorly understood. Considering the low
concentrations in which the strigolactones are active on
both organisms, it is reasonable to assume that a receptor-
mediated signalling mechanism is involved. For parasitic
plants this could be analogous to plant hormone perception
through receptors [54,55], for example, the perception
of gibberellins and auxin by receptors GID1 and TIR1
[56,57]. Indeed, in preliminary experiments, biotinylated
GR24 was used to detect a strigolactone binding
protein from membrane fractions of Striga hermonthica
[58]. The biological activity of the strigolactones as germi-
nation stimulants resides mainly in the bridge between the
C- and D-ring [59] (Figure 1). Strigolactone structure
function and the involvement of a receptor have not
been analysed for AM fungi. However, the strong and
rapid fungal cellular response to the strigolactones is
also suggestive of an efficient signalling amplification
system. Within an hour after the addition of GR24,
a strong modification of the shape and motility of
mitochondria is observed, associated with higher mito-
chondrial density and higher levels of respiration [35].
An important question is whether the CD-ring is essential
here also.
The appearance of the symbiotic plantfungus
interaction long before the hostparasitic plant interaction
raises the question of whether AM fungi and parasitic
plants respond to the same molecules using the same
mechanism. Considering how phylogenetically distant they
are, it would seem unlikely that they possess homologous
receptors and downstream signal transduction, but we can-
not exclude this possibility. Strigolactones have a strong
effect on mitochondrial activity in AM fungi [35], and the
activation of seed germination also involves an increase in
mitochondrial activity [60]. The obligate biotrophic nature of
AM fungi and Striga and Orobanche is indeed compatible
with a rigorous control of the process that uses the reduced
C stored in the propagating structures (spores and seeds),
that is, the mitochondrial catabolic activity. Although fun-
gal, plant and animal mitochondria differ in many respects,
the findings in animal cells that mitochondria are equipped
with hormone receptors and autonomous molecular machin-
ery to regulate mitochondrial gene expression [61,62] opens
up fascinating new research fields in plant and fungal
cell biology. If mitochondria are directly activated by
strigolactones, possibly through some conserved mechan-
ism, we can anticipate that many other rhizosphere
organisms are sensitive to strigolactones as well. Thus,
the biological significance of these allelochemicals in soil
ecology would go far beyond the boundaries of the parasitic
and symbiotic interaction discussed here.
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Vol.12 No.5 227
Strigolactones and host spectrum
Germination experiments with seed batches collected from
S. hermonthica and O. ramosa plants parasitizing several
different host species show that the parasites develop a
preference for the exudate of the host species they were
growing on [63]. If this is caused by differences in the
strigolactone composition of the exudates, this must mean
that small variations in the A-, B- and/or C-ring do have
some effect on the activity of the strigolactones because the
CD ring structure is the same for all known strigolac-
tones. However, strigolactones alone are not enough for
successful establishment of the parasitic interaction: stri-
gol, for example, was first isolated from cotton, a non-host
for Striga and Orobanche [64]. There are several other
plant species that also produce strigolactones and induce
germination of parasitic plant seeds but that are not a host.
Thus, host specificity is also determined at later stages by
other factors such as the haustorium-inducing factors,
incompatibility reactions or the presence of toxic metab-
olites [5,6567].
In contrast to parasitic plants, AM fungi have a broad
host spectrum. A relatively small number of fungal species
(150 described) can colonize 300 000 plant species. As
described above, some plant families such as the Brassi-
caceae have lost the ability to interact with AM fungi. In
line with this, no hyphal branching activity has been
detected in the root exudates of three Brassicaceae (Ara-
bidopsis thaliana, Brassica napus and Brassica oleracea)
[68], although it has been reported that Arabidopsis does
induce germination of several Orobanche spp. [69]. It has
not been assessed whether this is because of the presence of
strigolactones in Arabidopsis root exudate or other metab-
olites that are only active on Orobanche and not on AM
fungi. We are currently trying to identify the biosynthetic
origin of the Arabidopsis germination stimulant. In
addition to stimulants, there are also reports about inhibi-
tors in both the fungal as well as the parasitic plant
interaction that can affect host specificity. For example,
tomato mutants that have lost the ability to engage in
mycorrhizal colonization over-produce inhibitory phenolic
compounds [70]. In Brassicaceae, glucosinolates exuded by
the roots have been reported to be inhibitory to hyphal
growth of AM fungi [71]. In the non-host Beta vulgaris, root
exudates were found to contain neither stimulatory nor
inhibitory activity to AM fungi: co-culture of B. vulgaris
(non host) roots with Daucus carota (host) roots could not
revert the non-host status of B. vulgaris [72]. Furthermore,
germination and infection of parasitic plants has been
reported to be affected by inhibitors [73]. This illustrates
that in addition to the presence or absence of strigolac-
tones, other mechanisms are involved in the compatibility
of both interactions.
Strigolactone biogenesis
A rigorous evaluation of the importance of the
strigolactones for the interaction of plants with AM fungi
as well as parasitic plants, and their role in determining
host specificity can only be made using plants that have
altered or completely blocked strigolactone formation. In
principle, this can be achieved using inhibitors such as
fluridone and norflurazone [40,74] but these have the
228 Review TRENDS in Plant Science Vol.12 No.5

Figure 3. Unrooted phylogenetic tree of plant carotenoid cleaving enzymes, carotenoid cleavage dioxygenases (CCDs) and 9-cis-epoxycarotenoid cleavage dioxygenases
(NCEDs). Enzymes of cluster CCD1 (highlighted in blue) are involved in the production of volatiles such as b-ionone, whereas enzymes of the groups CCD7 (in green) and
CCD8 (in orange) are involved in the production of a plant branching inhibitor [76]. NCED enzymes are mainly grouped into two clusters: NCED1 (in pink) related to ABA
biosynthesis [75] and NCED4 (in yellow) with as yet unknown function. Finally, there is a specific cluster in rice (in grey) that also have unknown function. Plant species and
corresponding enzymes and accession numbers are: Arabidopsis AtCC1 (NM116217), AtCCD7 (NM130064), AtCCD8 (NP195007), AtNCED2 (NM117945), AtNCED3
(NM112304), AtNCED5 (NM102749), AtNCED6 (NM113327), AtNCED9 (NM106486); rice (Oryza sativa) OsCCD1 (AK066766), OsCCD7 (AK109771), OsCCD8 (AK58473),
OsNCED1 (AY838897), OsNCED4 (AY838900), OsNCED5 (AY838901), Oscrocetin (NM001069391), Osdioxygenase (NM001050764), Oslignostilbene1 (AK241374),
Osneoxhantin1 (AC074355); maize (Zea mays) ZmCCD1 (DQ100346), ZmNCED1 (vp14) (U95953); tomato (Solanum lycopersicum) LeCCD1A (AY576001), LeCCD1B
(AY576002), LeNCED1 (AJ439079), LeNCED4 (TC181718); pea (Pisum sativum) PsCCD7 (DQ403160), PsCCD8 (AY557332), PsNCED4 (AB080194); petunia (Petunia hybrida)
PhCCD8 (AY746977). Sequence accession numbers retrieved from GenBank. The sequences were aligned using the ClustalW program and the phylogenetic tree created
with the TreeView 3.2 program.

disadvantage that they also block carotenoid biosynthesis
in the aerial parts. Plants with more specific inhibition of
strigolactone formation could be obtained using mutant
screens or genetic modification of specific steps of the
strigolactone biosynthetic pathway.
The strigolactones were identified in the past as
sesquiterpene lactones [19,30,64], but it has recently been
shown in maize, sorghum and cowpea that the ABC-part of
the germination stimulants is derived from carotenoid clea-
vage [74]. Although the exact position in the carotenoid
pathway where strigolactone biosynthesis branches off from
the main pathway has not been identified yet, it is clear that
carotenoid cleavage is involved in germination-stimulant
biosynthesis because carotenoids are C40 molecules
whereas the strigolactones are C14 compounds (excluding
the D-ring) [74]. Carotenoid cleavage is a common biosyn-
thetic reaction that occurs in several biosynthetic pathways,
including the production of important plant signalling mol-
ecules. This includes the formation of the plant hormone
abscisic acid through the action of 9-cis-epoxycarotenoid
cleavage dioxygenases (NCEDs) [75] (Figures 2 and 3)
and the formation of an as yet unidentified plant hormone
involved in the control of plant architecture through the
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action of two carotenoid cleavage dioxygenases (CCDs) [76]
(Figure 3). A CCD is also involved in the formation of
apocarotenoid compounds upon mycorrhizal colonization
in the host root [77] (Figure 2). The role of these compounds,
known as cyclohexenone derivatives and mycorradicin, is
still unknown. For strigolactone biosynthesis, we have also
postulated how, after carotenoid cleavage, further enzy-
matic conversions are likely to lead to the production of
all strigolactones known to date [74] (Figure 2). Strigolac-
tones have also been detected recently, or at least suggested
to be present, in model plant species such as L. japonicus,
Medicago truncatula, tomato and rice (Oryza sativa)
[28,30,78]. Reverse genetics with these model plants and
the availability of extremely sensitive bioassays, such as the
hyphal branching assay of AM fungi [79] and the seed
germination assay of parasitic plants [74], should help to
further elucidate the strigolactone biosynthetic pathway.
Conclusion
The signalling role of strigolactones for parasitic plants as
well as the symbiotic AM fungi illustrates that signalling
in the rhizosphere can consist of complex networks of
interactions that are intimately regulated by biotic as well
 Review TRENDS in Plant Science
as abiotic factors. Seemingly unrelated facts discovered in
the past can now be integrated into a more general scheme
of interaction:
 Low phosphate in soil is favourable to AM symbiosis
[39].
 Phosphate starvation induces strigolactone production
[48].
 Strigolactones promote mycorrhizal colonization of host
plants [40].
 Strigolactones also promote parasitic plant infection
[19].
 Mycorrhizal colonization prevents parasitic plant infec-
tion through down-regulation of germination stimulant
production [52].
Future research is required to elucidate the mechanisms
by which strigolactone signalling is regulated and how
these signals are perceived by the responding organisms.
Strigolactone-defective plant mutants, or the modification
of strigolactone biosynthesis through metabolic engineer-
ing, will not only be essential to further evaluate their
importance in the plantplant and plantfungus relation-
ships described here, but will also be useful to see whether
other organisms use or abuse these signalling molecules. If
the mechanism of action of strigolactones turns out to be
conserved, the biological significance of these molecules in
rhizosphere signalling could be even larger than we can
now grasp.
Acknowledgements
We acknowledge funding by the Netherlands Organization for Scientific
Research (NWO; Vici-fellowship to H.J.B.), the European Commission
(the FP5 EU project Improved Striga Control in Maize and Sorghum,
INCO-DEV ICA4-CT-2000-30012; the FP6 EU Integrated Project Grain
Legumes FOOD-CT-2004-506223, both to H.J.B.), the Dutch Ministry of
Agriculture, Nature Management and Fisheries North-South programme
(to H.J.B.) and the French Ministry of Research to C.R. and G.B. J.A.L-R.
was supported by an EU Marie Curie fellowship (FP6-MEIF-CT-2005-
024345).
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