Host Recognition Strategies of Striga - A Parasitic Angiosperm
Host Recognition Strategies of Striga - A Parasitic Angiosperm
William Stump
Colorado State University
Fort Collins, Colorado 80523
Abstract. Parasitic angiosperms are unique life forms that are
parasitic to other higher plants. Many of these parasitic plants have
developed complicated host recognition strategies. This review will
focus on Striga, a genus of the Scrophulariaceae, that contains many
parasitic taxa of agronomic importance. Striga species are root
parasites and most are obligate parasites. Many Striga species have
narrow host ranges as a result of co-evolution with host plants in the
agroecosystem. Specificity is ensured by chemical signals from the host
plant. In addition to normal germination requirements common in many
angiosperms, Striga species require a chemical stimulation from the host
before germination can occur. These chemical cues have been identified
as strigol, and other analogs of this sesquiterpene. Also, a variety
of other artificial chemical compounds have been found to initiate
germination. Strigol is thought to induce germination via ethylene
biosynthesis. For haustorial initiation an additional unique chemical
signal is required.
INTRODUCTION
Parasitic angiosperms are unique life forms that are parasitic to
other plants. These plants have evolved independently in 20 plant
families, comprising some 3000-5000 species (Musselman, 1987).
Parasitic plant classification is based on several criteria.
Holoparasites lack chlorophyll and depend entirely on the host for
nutrients, minerals and water; examples include Cuscuta sp. and
Orobanche sp. Hemiparasites have chlorophyll and thus can fix CO2
depending on the host for water and minerals; examples here include
Striga sp. and mistletoes. Some parasites attack the shoot, others the
root. Parasites that require attachment to the host to complete their
life cycle are obligate parasites whereas facultative parasites can
complete their life cycle without the host. Despite parasitic plant
diversity, their common feature is the special host contact organ the
haustoria. With the haustoria, the parasitic plant is able to penetrate
the hosts epidermis and establish a connection.
Parasitic plants are a heterogeneous group being represented by
generalists, with a wide host range, and specialists with narrow host
ranges depending on their chosen co-evolutionary pathway (Musselman,
1987).
Though the number of parasitic genera is great, the bulk of the
research has been concentrated on agronomically important genera from
five families that include the following:
Scrophulariaceae: Striga
Orobanchaceae: Orobanche
Cuscutaceae: Cuscuta
Visacaceae/Loranthaceae: Mistletoes
Seedlings of obligate parasites, in order to survive, must quickly
find a suitable host or they will soon die. To accomplish this,
parasitic life forms have evolved complicated host recognition
strategies. These strategies include host chemical cues for germination
and haustoria formation, responses to light environment, and reliance on
avian seed predators to disseminate seeds to appropriate hosts
(Musselman, 1980; Calder and Berhardt, 1983). This review will focus on
Striga, a genus that contains many agronomically important weeds. This
genus causes considerable yield losses in various crops in tropical and
subtropical countries. The majority of Striga species are root
hemiparasites and most are obligate parasites. The most studied are S.
asiatica (L.), S. hermonthica (Del.) pests of graminous crops, and S.
gesneriodes (Willd.) which parasitize legumes (Musselman, 1980; Parker
1991). Many Striga species have narrow host ranges as a result of co-
evolution in the agroecosystem. Host specificity is ensured by chemical
signals from the host plant.
Striga Life Cycle
The life cycle of Striga is composed of five stages, as follows:
1. Germination (after seed preconditioning)
2. Haustorial initiation
3. Penetration of host tissue
4. Physiological compatibility
5. Parasite growth and maturation preconditioning
Prior to germination Striga must undergo an after-ripening period
before it will respond to any germination stimulants. This after-
ripening is analogous to other angiosperm seeds that possess an innate
dormancy. For most of the species studied, seeds require certain
temperature and moisture regime of a period of about two weeks. It is
thought that this period is necessary to remove phenolic compounds that
act as germination inhibitors (Musselman, 1980). Subsequent to the
after-ripening, seeds of Striga require a period of conditioning before
responding to germination stimulants. Typically, warm moist conditions
are required for about a week before maximum germination will take place
after receiving the host stimulatory cue.
The Germination Process
The seeds of Striga are very small, measuring 0.15 x 0.31 mm, so it
is quite obvious that Striga seeds lack the reserves for sustained
periods of growth before host attachment. For successful host
attachment germination must take place within 3 to 4 mm of the host root
since Striga radicles can manage only 2-4 mm (Ramaiah et al., 1991). To
compensate for these biological restrictions Striga produces up to
450,000 seeds per plant, with a persistence in the soil of up to 10
years (Eplee, 1992). The most important, and evolutionarily complicated
adaptation, is Striga's requirement of a germination stimulant from a
nearby host.
Germination Stimulation
Many chemicals have been discovered that promote germination in
Striga. These chemicals include ones that are naturally occurring in
plant root exudates, various synthetic plant hormones, and a variety of
other derived compounds. Because of potential control benefits, many
researchers have attempted to isolate and identify natural host
stimulants. It has been found that host plants produce a mixture of
stimulatory compounds with one compound being predominant over the
others (Worsham, 1987; Weerasuriya et al., 1993). These compounds have
been found to be very active and are present in root exudates at
extremely low levels. This potent behavior has led some researchers to
speculate that these germination stimulators represent a new class of
plant hormones (Cook et al., 1972; Siame et al., 1993). Unfortunately,
the low concentrations and instability of these compounds has made
isolation and identification difficult.
The first naturally occurring germination stimulant characterized
was strigol, a sesquiterpene isolated from cotton, a non host plant
(Cook et al., 1972). Strigol has activity in the soil solution at
concentrations as low as 10-15 mol m -3. The molecule, whose
absolute structure was established in 1985 (Brooks et al., 1985),
consists of four rings: a six-carbon ring (A), a five-carbon ring (B),
a four-carbon lactone ring (C) coupled to another lactone ring (D) by a
=C-O- connecting unit. (see figure 1). Once an active structure was
established, many strigol analogs have been synthesized along this ABCD
ring structure, and tested for activity. These compounds were termed
"GR" compounds and several had fairly good activity (Worsham, 1987).
Work by Mangnus and Zwannengurg (1992) along these lines has shed some
light on the molecular activity of these compounds. The research
suggests the importance of the linkage between the two lactones is
crucial for activity.
Identification of Host Germination Stimulants
Many attempts have been made to isolate Striga germination stimulants
from true host plants. The first host derived stimulant was sorgoleone
from Sorghum bicolor hydrophobic root exudates (Chang et al., 1986;
Netzly et al., 1988). The compound is an unstable dihydroquinone which
is rapidly oxidized to a stable inactive quinone (see figure 2). Unlike
strigol, sorgoleone is hydrophobic and not as active with activity down
to 10-7 M. Chang et al. (1986) hypothesized that the ephemeral nature
and limited mobility of the compound was capitalized by Striga to ensure
germination in close proximity to the host root.
However, in 1991 an additional new stimulant, sorgolactone, was
isolated from water soluble sorghum root extracts (Hauck et al., 1991).
This new compound is very similar to strigol in structure, solubility,
and activity on Striga germination (figure 2)
Figure 2. Structures of (a) strigol, (b) sogolactone, and (c)
sorgoleone..
Recent work done on characterizing resistant and susceptible sorghum
cultivars on agar gel assay (Hess et al., 1992) and a dilution assay
(Weersuriya et al., 1993) found great differences in the amount of
germination stimulators for Striga asiatica present in sorghum root
extracts. The resistant cultivars, where resistance is based on low
stimulant production, produced the same amount of sorgoleone as
susceptible cultivars. These findings cast a shadow on the importance
of sorgoleones as Striga stimulants. It was concluded that since the
agar gel assays measured more water soluble stimulants and correlated
well with strigol, that the main germination stimulant was the more
water soluble sogolactone rather than sorgoleone (Hess et al., 1992).
An additional Striga stimulator was found in cow peas, Vigna
unguiculata, which is parasitized by Striga gesnerioides a species that
has evolved to parasitizes mainly legumes. Legumes are frequently used
as trap crops for Striga sp. that parasitize cereals since they are non
hosts. Cow peas, produce a variety of Striga stimulators. The most
prevalent compound was identified as alectrol, a strigol analog (figure
3)
Figure 3. Alectrol (proposed structure)
.
It was not until 1993 that strigol was isolated from the Striga host
plants maize (Zea mays L.) and proso millet (Panicum miliaceum L.) by
Siame and others (1993). Very small amounts of strigol was also found
in sorghum but the major stimulant was thought to be that of
sorgolactone. The authors felt that identification of strigol in true
host plants took so long because most studies utilized sorghum root
extracts of which strigol is only a minor component. Also, strigol is
present in very low concentrations in host root extracts making
isolation difficult.
Other Chemicals that Stimulate Striga Germination
In addition to natural host exudates and analogs of strigol a number
of unrelated and diverse chemicals have been found to stimulate Striga
germination in vitro. These include several growth hormones; kinetins,
zeatin, and ethylene (Worshum, 1987). The use of ethylene is the
backbone of the US witchweed (Striga asiatica) eradication program.
Ethylene injected into the soil has been found to promote germination up
to 90% to a depth of 30 cm at a concentration of 10-1 µl/L (Eplee,
1992). Somewhat less efficacy of ethylene was found on the stimulation
of Striga hermonthica in Africa due to the drier soil conditions (Bebawi
and Eplee, 1986). Other chemicals that induce germination include
scopletin, inositol, and sodium hyperchlorite. It is not clear at this
time how these various chemicals can stimulate germination (Worshum,
1987, Igbinnosa et al., 1992).
Mechanisms of Germination Stimulation in Striga
Mechanisms by which strigol and its analogs stimulate germination in
Striga is just recently starting to unfold. Much of the work has
concentrated on the role of ethylene on germination. Since ethylene
promotes germination in parasitic plants such as Striga, as well as many
other non parasitic angiosperms, it has been hypothesized that strigol
stimulates germination by promoting ethylene biosynthesis (Logan and
Stewart, 1991). This could also possibly explain how the diverse
artificial chemical stimulants could promote germination by indirectly
initiating ethylene production via a wound response (Gabbar et al.,
1993). Strigol stimulated ethylene biosynthesis in preconditioned
Striga asiatica seeds within three hours of application and prior to
radicle elongation (Gabbar et al., 1993). Both germination and ethylene
production were inhibited by aminoethoxyvinyl glycine (AVG), an
inhibitor of ethylene biosynthesis (Logan and Stewart, 1991) and by 2,5-
norbornadiene, an inhibitor of ethylene action (Gabbar et al., 1993).
Addition of an ethylene biosynthesis intermediate, 1-amino-cyclopropane-
1-carboxylic acid (ACC), was found to override the inhibitory effect of
AVG (Gabbar et al., 1993). Strigol is thought to trigger activation
and/or synthesis of ethylene forming enzymes for subsequent conversion
of ACC to ethylene (Gabbar et al., 1993). Ethylene has been found to
stimulate germination in a number of plant species and is thought to
initiate the biochemical cascade leading to germination (Logan and
Stewart, 1991).
There has been great interest in using a stimulant as a method for
control of striga in a cropping situation. Introduction of a
germinating agent before a crop is planted can reduce striga populations
via suicide germination (Eplee, 1975). Since strigol is such a
complicated molecule, requiring 12 to 20 steps to synthesize, a sizable
amount of work has gone into determining which parts of the molecule
confer activity in the hopes of finding a simpler to synthesize compound
(Vail et al., 1990; Mangnus et al., 1992). Taking the ABCD ring
structure of strigol, various analogs were made along the ABC portion of
the ring. It was found that the D portion of the molecule was necessary
for activity in conjunction with A and or B with C not as important for
activity (Mangnus, et al., 1993). Work has not been conclusive in this
area and the absolute molecular mechanisms have yet to be established.
Haustoria Initiation
Host recognition in parasitic angiosperms is typically presented at
two levels, depending on the level of parasitism. For obligate
parasites such as Striga, where a parasitic relationship is required for
completion of life cycle, host recognition is determined by stimulation
of germination via a chemical cue from the host as discussed in the body
of this paper. For facultative parasites, where parasitism is not
necessary to complete it's life cycle, host recognition is accomplished
by stimulation of haustoria formation by a chemical cue from the host
(Steffens et al., 1986). The first haustoria inducers isolated for the
facultative root parasite Agalinis purpurea were phenylpropanoids named
xenogin A and B extracted from Astragalus gummifer a non host plant
(Lynn et al., 1981) However, since these compounds were extracted from
aerial portions of Astragalus gummifer it's biological relevance was in
question. Investigating exudates from Lespedeza sericea, a true host of
Agalinis purpurea , a pentacyclic tritriterpenehaustorial named
soyasapogenal was found to be a haustorial inducer (Steffens et al.,
1986). However its chemistry is quite different from the
phenylpropanoids and is not as active and may depend on other yet
identified materials for full activity (Steffens et al., 1986).
It has been argued that host recognition in obligate root parasites
such as Striga is by chemical cues for both seed germination and
haustoria formation (Musselman, 1980). Indeed, the fact that nonhosts
such as cotton and cowpea both can stimulate Striga germination but not
allow for a parasitic connection illustrates the need for an additional
chemical cue. Striga asiatica, haustoria initiation is in response to a
single quinone, 2,6-dimethoxy-p-benzoquinone (2,6-DMBQ) found in sorghum
root extracts (Chang and Lynn, 1986). However, 2,6-DMBQ is not found in
root exudates, its presence requiring vigorous shaking of root tissue,
which indicates its within the host root tissue (Chang and Lynn, 1986).
A byproduct of lignin degradation by fungi with extracellular lactases
is also 2,6-DMBQ. Coupled with the fact that Striga utilizes cell wall
degrading enzymes, it has been suggested that Striga lactase activity
releases quinones from the host root that stimulate haustoria initiation
(Stewart and Press, 1990).
However, calling haustoria initiation in Striga a host recognition cue
is somewhat misleading. Once the parasite has germinated it had better
be in the presence of a suitable host or it will soon die, further host
selection at this juncture is pointless. This is the basis of the
control technique of "suicide germination". I propose that this
secondary chemical cue is strictly for the detection of the proximity of
the host root. A time course study of establishment of Striga asiatica
on susceptible sorghum roots by Ramaiah et al (1991), found that 63% of
the Striga seeds germinated within 24 hours of inoculation of sorghum
roots. However a small percentage actually establish a parasitic
connection with the host. Timing of haustoria formation is critical in
the establishment of parasite to host connection.
Evolutionary Significance of Germination Stimulators
The purpose of these excreted compounds from the hosts perspective is
still a question That is, if one is to believe all plant secondary
compounds have a biological purpose. Some research has indicated that
these compounds are allelochemicals. Sorgoleone has shown some
herbicidal activity and may function in allelopathy. However no work
has been done to investigate the effects of strigol and it's analogs for
possible plant defense mechanisms. The use of host defense chemicals as
feeding cues is not a new evolutionary idea because of its frequent
occurrence in insect herbivory. Atsatt (1977), proposed similar
patterns would be found in parasitic plant relationships. Parasitic
plants host relationships was likened to three evolutionary patterns of
insects response to host plants: resistance to host chemistry, use of
host defense chemicals as feeding cues, and secondary utilization of
host defense compounds. Though not as much work has been undertaken in
these areas, there is growing evidence for this hypothesis.
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