The Biology and Distribution of Parasitic Plants within the Orobanchaceae: An
Overview of Secondary Plant Compound Involvement
Patrick Miller (4-22-94)
Colorado State University
Fort Collins, Colorado 80523
Abstract:
Evolutionary ecologists and behaviorists are beginning to realize
that parasites, whether conspicuous or not, influence the workings of
nature much more profoundly than most people suspected. Even within
the context of parasitic plants, where species such as Orobanche become
a prominent feature in agro-ecosystems, the ecological impact(s) as a
result of these plants are not well understood. The objective of the
paper presented here is two-fold. The first goal rests in the description
of Orobanche species biology and distribution; and the second, in
appraising the information available, with respect to the production of
plant compounds, which enable Orobanche species to exhibit the
distribution and influence on crop plants they presently have. Some of
the salient features of these organisms which influence their occurrence
and success in the environment include; seed dormancy mechanisms,
preconditioning (imbibition) requirements, detection and germination
stimulant response, and in vivo enzyme activities during host-parasite
interactions. As discussed in the text, the life-cycle of Orobanche species
is a complex and dynamic relationship between host, environment,
edaphic and biotic factors. Each of the many individual stages through
which these parasitic organisms pass, contain a complement of stimuli
with which the organism must contend. As much of the research
performed thus far has illustrated, the chemicals produced by the
parasitic organism are often done so in the interest of the parasitic
plant itself. Although a tremendous amount of effort has been
expended in exploring these parasitic plants, it appears as though the
involvement of space and time on these interactions, has not been
examined to the extent it should. This fundamental information is
needed if we are to develop effective control strategies against parasitic
plants that threaten agricultural production.
Forward:
The objective of the paper presented here is two-fold. The first
goal rests in the description of Orobanche species biology and
distribution; and the second, in appraising the information available,
with respect to the production of plant compounds, which enable
Orobanche species to exhibit the distribution and influence on crop
plants they presently have. A famous biologist once called nature an
evolutionary play set in an ecological theater (Holmes, 1993). This
biologist went on to say that most ecologists in the audience would
regard the parasites as minor players, simply wandering the outskirts of
the stage, contributing nothing more than a trivial part.
Evolutionary ecologists and behaviorists are however, beginning
to realize that parasites, whether conspicuous or not, influence the
workings of nature much more profoundly than most people suspected.
As the discussion which follows will illustrate, because parasites
(parasitic plants) make difficult experimental subjects, information
regarding their importance in an agronomic or ecological setting is
difficult to come by. Many parasitic plants have intricate life-cycles
involving several host species, or different life-cycles on differing host
species. Additionally, most ecologists haven't learned to think about
parasitism until recently, primarily because of the difficulties
surrounding the non-free-living parasite's nature.
Even within the context of parasitic plants, where species such as
Orobanche become a prominent feature in agro-ecosystems, the
ecological impact(s) as a result of these plants are not well understood.
Although parasites have been documented as playing a striking role in
the ecology of their hosts, (Reuter, 1986) particularly by controlling
population sizes, this phenomena is of more agronomic than ecological
concern within the context of this discussion (i.e., manipulated
crop/host populations). Thus, at this time, researchers have many more
questions than answers.
Introduction:
Over 3000 species of flowering plants utilize a parasitic mode of
nutrition, and yet, basic information regarding their physiology and
biochemistry is limited. Broomrapes (Orobanche spp.) which belong to
the family Orobanchaceae are obligate parasitic flowering plants.
Parasitic angiosperms are generally separated into the two broad
categories of either holoparasites and hemiparasites. Holoparasitic
species are always obligate parasites, are absent of chlorophyll and
have little independent capacity to assimilate or fix carbon and/or
inorganic nitrogen (Stewart and Press, 1990). Hemiparasites on the
other hand, may be facultative or obligate, contain chlorophyll, and are
traditionally thought to rely on their host only for water and minerals.
Tuohy, et. al. (1986) have suggested that the extent to which
parasitic plants are dependent on their hosts must somehow be related
to their own photosynthesizing abilities. Parasitic flowering plants are
further subdivided on the basis of their site of attachment to the host.
Stem parasites, such as the holoparasitic dodders and the hemiparasitic
mistletoes, as well as root parasites, such as the holoparasitic
broomrapes and hemiparasitic witchweeds exist. The distinguishing
feature of all parasitic plants is the haustorium, a novel organ that
functions in attachment, penetration, and solute transfer (Kuijt, 1977;
Visser and Dorr, 1986; Stewart and Press, 1990).
Background:
Their main center of distribution is the Mediterranean region,
where large areas are heavily infested. Other regions with similar
climatic conditions (California, Western Australia, Cuba) have also
been invaded (Musselman, 1986). Some species can be found in arid or
semiarid environments, and others are found as far north as Sweden
(Linke, et. al., 1989). Of the 100 or more species in the genus
Orobanche, only a few are of economic importance as weeds in cropping
systems. These parasitic plants vary greatly with respect to host range,
and parasitize a wide range of plant families (Asteraceae, Fabaceae,
Solanaceae, Apiaceae, Cucurbitaceae).
Due to the complete devastation caused by Orobanche in many
areas, production methods often need to be modified. These
modifications can entail the use of fallow cropping systems, or in
extreme cases, completely abandoning fields from crop production.
Additionally, the biology and host specificity of Orobanche, warrant the
implementation of special forms of cropping systems or management
tactics. Thus far, no single means of control has been identified as
being sufficiently efficient or economical.
Species, Distribution and Hosts:
Table 1, (adapted from Foy, et. al., 1989, appears on the following
page) indicates the hosts associated with a particular Orobanche species.
Figures 1 and 2, (taken from Linke, et. al., 1989, appear on the following
page) illustrate the geographical distribution of the four most prevalent
and economically important Orobanche species (O. aegyptiaca and O.
ramosa, in Figure 1; and O. cernua and O. cumana, in Figure 2).
Table 1. The economically important broomrapes and the crops which
they parasitizea.
Figure 1. Species distribution and hosts
for O. aegyptiaca and O. ramosa.
Figure 2. Species distribution and hosts
for O. cernua and O. cumana.
Biology:
Most species of Orobanche are annual and are reproduced by seed.
With regard to parasitism, the host-parasite relationships throughout
the genus are of a highly specialized nature. A diagrammatic
representation of the complexity of this relationship is illustrated below
in Figure 3. These relationships are modified by climate and man.
Factors like host, soil or predators can play an additional role (Linke,
et. al., 1989).
Figure 3. Life-cycle of Orobanche species.
Seeds:
Seeds of Orobanche are among the smallest in plant kingdom.
Seed weight ranges from 4-9 x 10-3mg, and size varies according to
species. Position within the inflorescence also affects germinability,
dormancy and seed size, with smaller seeds being found nearer the top
of the spike. The seed coat shows characteristic thickenings at the
surface which may help in dispersal by wind and water. Seeds are
produced in large quantities, 500-5000 per capsule being most common,
with more than 100 capsules per plant seldomly found. Plants of O.
crenata (a robust species), can produce several hundred thousand seeds,
while the smaller species (e.g., O. ramosa) may produce only 5,000-
20,000 seeds per plant. The seeds however, can remain viable in the
soil for more than 10 years (Linke, et. al., 1989). This feature alone
makes the parasitic plants an extremely difficult intruder in agro-
ecosystems.
Germination and attachment:
The segment of parasitic plant research historically receiving the
most attention is the area of germination stimulation. Presumably, in
the attempt to isolate an active analog which can be used as a control
measure (forcing germination of parasitic plants) in cropping
situations. Germination stimulants have however, proved to be elusive
for three major reasons. Firstly, they are active at extremely low
concentrations. Secondly, their presence in a complex media such as
soil makes their isolation difficult. And finally, the structures which
have been successfully isolated and identified are quite fragile or
transitory in the soil environment (Stewart and Press, 1990).
Nun and Mayer (1993) recently indicated that freshly harvested
seeds remain dormant for several days or months depending on species
and environment. In addition, these researchers indicated, that even
under favorable conditions, germination takes place only in the
presence of a germination stimulant released by roots of the host plant.
Spread of stimulant in the rhizosphere depends on soil water content.
Temperature seems to be a key factor for Orobanche germination
and development. Temperatures around 15-25oC are optimal for O.
crenata and O. ramosa, while below 5oC and above 30oC only a few
seeds will germinate and develop. Upon germination a hyaline, root-
like structure, the germ tube, expands out of the testa. It can reach a
length of 3-4mm with a diameter of 0.15mm. For this reason, only
seeds in the immediate vicinity of the host roots (3-4mm) can lead to
parasitism. The germ tube shows a positive chemotropy in the vicinity
of the host root, (i.e., it grows in the direction of the host root).
With respect to seed preconditioning (imbibition), Nun and Mayer
(1993) clearly illustrated that seeds which are not exposed to a
germination stimulus are able to remain viable for long periods without
damage. However, they also showed that seeds which start to
germinate, but do not reach a host show indications of stored nutrient
exhaustion and the likelihood of death. If the germ tube reaches the
host root its tip thickens and attaches itself to the root surface. The
thickening is known as the appressorium (from Lat. apprimere=to
attach, to fix).
Tubercle and haustorium:
The appressorium connects itself by means of enzymatic
degradation and mechanical penetration of the host root vessels. Both
of these phenomena have been documented in recent experimental
procedures, however, the preponderance of evidence at this time
supports the involvement of enzymatically mediated degradation
(pectin methylesterase, Ben-Hod, et. al., 1993; and cellulase, xylanase,
and poly-galacturonase, Singh and Singh, 1993) in the infection of host
plants by Orobanche. This connecting tissue is the haustorium (from
Lat. haurire=to drink) (Linke, et. al., 1989). After contact between
the appressorium and the host vessels is made, the former is henceforth
known as the tubercle. (from Lat. tuberculus=small hump, -knob). This
organ, yellow to orange in color, now starts to enlarge. The mature
tubercle is 0.5-2.5cm thick in most species, though thicker in some (up
to 5cm). With this organ the parasite withdraws water, mineral and
organic compounds from the host (Kuijt, 1977; Visser and Dorr, 1986;
Stewart and Press, 1990).
Shoot development and emergence:
After the formation of crown roots on the tubercle a bud develops
(bud stage) which later forms a shoot. The main shoot is sparsely
covered with scaly leaves. In some species branching of the shoot is
normal (e.g., O. aegyptiaca, O. ramosa), whereas in others it is rare (e.g.,
O. minor, O. crenata, O. cernua). During the underground stage of its
life-cycle Orobanche accumulates carbohydrates; visible growth being
comparatively slow. But the reserve of carbohydrate enables the
parasite to elongate its shoot, emerge from the ground, and produce an
aerial shoot and flowers within a very short period.
Duration of shoot development and emergence bears a close
relation to the soil temperature, the nutritional status of parasite and
crop, and to a lesser extent the identity of the host plant itself.
Depending on environmental conditions the underground phase of the
Orobanche life-cycle ranges from 30 to over 100 days. The whole life
cycle from seed germination to seed production requires about 3-7
months.
Crop Damage:
Mode of action and symptoms:
The growth of the parasite occurs at the expense of water, mineral
and organic compounds from the host. The tubercle and underground
shoot accumulate carbohydrates and thereby become a strong sink for
all plant nutrients. Effect on host plant growth becomes noticeable
when the parasite emerges from the soil. Growth of Orobanche shoots is
most rapid during that period and it induces a lack of carbohydrate in
the host roots. Osmotic pressure in the host is reduced to an extent
that symptoms like wilting and drought stress can occur.
Kind of damage:
Damage to an infested host crop is through reduction in yield of
both seed and straw. Yield reduction occurs after any infestation as the
parasites' dry matter is produced from the assimilates that should have
been used by the host itself. Reduction in quality occurs in several
crops such as tobacco, sunflower, tomatoes, carrots, cabbage and
eggplants.
Economic importance:
Yield reduction is dependent on the timing and severity of
infestation. Yield losses vary and generally range from 5 to 100%
(Stewart and Press, 1990). The loss. averaged across all broomrape
species, is approximately 34%. O. cernua probably causes the most
widespread damage of all Orobanche species, as it affects about 7
million hectares of sunflower in eastern Europe and Near East. O.
crenata and O. aegyptiaca occur in legume fields of West Asia and North
Africa, threatening production of these crops in an area of nearly 4.4
million hectares. Another 2.6 million hectares of solanaceous crops like
tomato, potato, tobacco and eggplant are threatened by O. ramosa and
O. aegyptiaca in the same region (Linke, et. al., 1989).
Discussion:
As illustrated in Figure 3, the life-cycle of Orobanche species is a
complex and dynamic relationship between host, environment, edaphic
and biotic factors. Each of the many individual stages through which
these parasitic organisms pass, contain a complement of stimuli with
which the organism must contend. As much of the research has
illustrated, the chemicals produced by the parasitic organism are often
done so in the interest of the plant itself (i.e., the presence of
germination inhibitors within seed to ensure some level of dormancy; a
strict period of optimum conditions prior to the release or dissipation
of specific germination inhibiting compounds; detection of the
appropriate type and concentration of germination stimulant; and
finally the collaboration of these events, in some spatial and temporal
framework). Although a tremendous amount of effort has been
expended in exploring these parasitic plants, it appears as though the
involvement of space and time on these interactions, has not been
examined to the extent it should. This fundamental information is
needed if we are to develop effective control strategies against parasitic
plants that threaten agricultural production.
Conclusions:
The primary focus of this paper was in the agronomic impacts or
ramifications as a result of Orobanche species exploitative abilities. The
broader, ecologically-based questions of how these interactions began
and why they have perpetuated remains. However, some biologists
have suggested that parasites may be the reason organisms bother to
reproduce sexually (Holmes, 1993). Along these same lines,
evolutionary biologist Bill Hamilton (Univ. of Oxford), suggests that sex
itself may have evolved because it reshuffles genes, thus helping
animals and plants resist parasites. Some support for this theory is
available for animals, in the form of a snail species found in New
Zealand which reproduces sexually in habitats where it is heavily
parasitized, but asexually where parasites are scarce.
Until recently, biologists and parasitologists believed that over
time, parasites and their hosts always evolved a kind of truce, in which
the parasites become more benign and the hosts become more tolerant
of them. Since parasites get both food and shelter from their host, any
parasite active enough to kill its host, would be committing suicide by
destroying its own habitat. Over the past ten years or so, however,
evolutionary biologists have largely discarded this alternative in favor
of a more complex one. Often, virulent parasites harm the host because
they are reproducing so rapidly. Such parasites may be unable to treat
their host in a gentle fashion without sacrificing in fewer offspring.
Researchers have illustrated no single best solution to this trade-off
between reproductive rate and longevity.
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