Herbologia, Vol. 14, No. 2, 2014
10.5644/Herb.14.2.07
BIOLOGICAL CHARACTERISTICS OF SOME PARASITIC
FLOWERING PLANTS
Milan Blagojević, Branko Konstantinović, Nataša Samardžić,
Milena Popov, Bojan Konstantinović*
University of Novi Sad, Faculty of Agriculture Novi Sad, Serbia
*Corresponding author: [email protected]
Abstract
Evolutionary conditions may favor development of parasitism in
practice. Orobanche spp. (broomrape) is holoparasitic flowering plant at
the root of a large number of crops that greatly reduce the yield in dry,
warm, temperate and semi-arid regions. The problem of pathogenic organisms is focused primarily on fungi, nematodes, bacteria and viruses.
These organisms certainly cause economically significant damages on
plants, and the fact that parasitic flowering plants are economically significant pathogens can be surprising. Roots of parasitic plants develop primarily on annual plants on which parasitic seedlings form haustoria and thus
gain a functional root system. In order to create connection between the
host and the parasite, some kind of stimulus is needed. The substance for
stimulation of connecting the host and the parasite is highly unstable, so
the distance between the parasite seed and the root of the host plays a vital
role in creating a contact. Cuscuta campestris Yuncker – field dodder has
always been known as a plant without root and chlorophyll, i.e. parasitic
plant that is completely dependent upon the host. It is generally accepted
that water and inorganic nutrients are absorbed through the xylem between
the host and the parasite, and organic compounds are transported through
the phloem of the host, so that the parasite adapts it by phloem connections. This view has been accepted by almost all reference works and textbooks. The research has proved the existence of chlorophyll A and B in
very small quantities in Cuscuta campestris in relation 2.5:1.
Keywords: parasitic flowering plants, Orobanche, Cuscuta, holoparasites, hemiparasites.
Introduction
The first association problem of pathogenic organisms is directed
to fungi, nematodes, bacteria and viruses. These organisms certainly lead
Blagojević et al.
to economically significant damages of plants, and the fact that parasitic
flowering plants are also economically significant pathogens can be surprising. Parasitic plants are angiosperms (flowering plants) that are directly linked to other plants by haustoria. Haustoria are root modifications that
form morphological and physiological bonds between the parasite and the
host. Parasitic plants (originating from Greek word para - beside and zitos
– guard oneself) are organisms that cause parasitic plant diseases. These
are predominantly heterotrophic organisms, because they feed by ready to
eat food that they take from either living cells or dead organic matter. Only
a limited number of autotrophic organisms adapted to parasitic way of life.
Between parasites and saprophytes (sapro - rot, phyton - plant), there is
a great number of transitional forms, and among them there are no clear
boundaries. Some authors use this name to mark any agent of plant diseases, either of parasitic or non-parasitic nature. Therefore, it would be a
broader concept in relation to parasite which is of biotic nature. However,
phytopathologists often use the term pathogen, mainly for parasitic organisms. If the symptoms of disease are created on the host, then it is pathogen,
as well as parasite. Until now, great number of parasitic organisms was
identified on plants. For example, so far in North America there are about
8.000 parasitic fungi, 300 bacteria, 500 viruses, 75 species of organisms
that look like mycoplasma and about 3.000 described parasitic flowering
plants. Parasitic weed species, known as broomrape - Orobanche cumana
Wallr. is one of limiting factors in sunflower production, as well as in other
world countries. Genetic resistance in combination with herbicides is the
best manner for control of this weed species (Eizenberg et al., 2006; Rubiales et al., 2009; Fernandez - Martinez et al., 2010). Even beside possible control, there is significant increase of infected areas. This parasitic
weed originates from Russia, and nowadays is widely spread in Eurasia,
including Black Sea region (Antonova et al., 2009). In Serbia, presence of
broomrape has also been confirmed (Maširević and Medić-Pap, 2009), as
well as on the territory of Romania (Pricop et al., 2011), Turkey (Demirci and Kaya, 2009), Spain (Fernandez-Martinez et al., 2009), Israel (Eizenberg et al., 2003), and it has recently been also discovered in Africa
(Amri et al., 2012). Certainly that intensive exchange of sunflower seeds
between countries in the world, as well as small broomrape seed enable
fast spread of this weed species. High genetic resistance of commercial
sunflower hybrids to this weed species in Argentina could be potential answer to high distribution of this weed species (Cantamutto et al., 2012).
Parasitic flowering plants, such as species of the genus Cuscuta L. (dod-
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Biological characteristics of some parasitic flowering plants
der) and Orobanche L. (broomrape), quantitatively do not have significant
number in relation to total weedy vegetation of Serbia that numbers 1,009
species (Kojić and Vrbničanin, 1998). Cuscuta genus includes over 100
species, distributed in moderate and warmer regions of the world. In vegetation Serbia, represented are only 10 species of this genus (Kojić and
Vrbničanin, 2000).
Species of parasitic plants
Unlike ordinary weeds, parasitic plants are heterogeneous plant organisms that are not able to synthetize sufficient nutrients need for their
development, due to which they lodge to other, host plant out of which
they extract nutrients through structures called haustoria that anatomically
connect binding channels of two plants (Konstantinović, 1999).
There are two basic types of parasitic plants that can be distinguished: parasites of stem and parasites of root. Stem parasites occurred in
several families, and pathogens are some mistletoe and field dodder (Cassitha and Cuscuta). Stem parasites are more frequent and are found in different taxonomic groups. Some of economically important stem pathogens
belong to the family of flowering plants, Orobanchaceae. Holoparasite
and hemiparasite species differ according to the degree of dependence of
parasites on the host plant. Hemiparasites can be obligatory and facultative
parasites. Optional (facultative or semi-) parasitic weeds contain chlorophyll and can survive without host. Facultative parasites or necrotrophs
held mostly on dead organic matter (saprophytic phase), and only a part of
development cycle they spend on plants (parasitic phase). From the other
hand, complete (obligatory or parasitic) weeds, demand host for survival.
Obligatory parasites can develop only on alive tissues of the host plant.
Hemiparazites contain chlorophyll during their growth, thus being photosyntetically active, and uptake water by binding with the host by haustoria. Holoparazites lack chlorophyll i.e. they are photosyntetically inactive
and therefore they must rely on the host xylem and phloem content. All
holoparasites are obligatory parasites. Although these definitions imply
absolute and partial categorization, some parasitic plants are intermediators between hemi- and holoparasitic plants, e.g. Cuscuta (dodder).
Morphological characteristics. On some stem parasites such as
Cassitha (mistletoe) and Cuscuta (dodder), vegetative part consists exclusively from stem and rudimentary leaves. Opposite to this, numerous photosynthetic hemiparasites of root will not be accepted as parasites because
they are green with completely formed leaves. As the level of parasitic
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Blagojević et al.
dependence grows (evolution from hemiparasites to holoparasites), great
changes occurred in morphology of parasitic plants. The best example of
evolutionary phase from hemi- to holoparasites can be seen between different representatives of the family of flowering plants (Orobanchaceae).
Orobanchaceae (flowering plants)
This family includes the greatest number of genus (90) and species
(about 1800) of all families of parasitic flowering plants. In Serbia there
are 26 different broomrape species, 56 varieties and 226 forms that make
total of 308 taxa (Maširević and Medić-Pap, 2009). In the past hemiparasitic members of this family have been classified as a part of Scrophulariaceae family, while holoparasitic members have been included in
Orobanchaceae family. The most recent molecular phylogenetic studies
that have included both hemi- and holoparasites show that Orobanchaceae
are monophyletic – i.e. they originate from a common ancestor, and that
evolutionary line is offspring of non-parasitic Scrophulariaceae. In further
text, two economically most important genus, Striga and Orobanche are
described separately, with similarities and differences of their life cycles.
Orobanche L.
The genus Orobanche contains about 150 species of holoparasites
that attack the root of the host. These plants are known for their English
names ‘’broomrape’’, because it was thought to grow as tubers (“rapum”)
from broom (the common name for legumes Cytisus). This genus reaches
its greatest diversity in Mediterranean climate and north Asia. The majority of economically significant pathogenic species are of ancient origin.
Molecular proves suggest that Orobanche is not monophyletic, so that other generic terms can eventually be applied. The main families of host for
parasitic Orobanche are legumes, nightshades (eggplant, tomato, tobacco,
potato, but not paprika), then squires (carrot, parsley, celery), brassicas
(cabbage, cauliflower) and composites (lettuce, sunflower). Control is difficult due to seed dormancy in the soil (more than five decades), tiny seeds
(smaller than width of the human hair), fertility (thousands of seeds per
plant), as well as due to underground phases (seed germination) under soil
and lives as parasite host before it emerges and becomes evident. Populations that naturally occur in red clover (Trifolium pratense) and carrot
(Daucus carota subsp. Gummifer), show different host specificities, indicating possibilities of fast adaptation. There are numerous studies on hosts
that attack Orobanche species. It has been shown that O. ramosa L. can
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Biological characteristics of some parasitic flowering plants
parasitize plants in 11 different dicotyledonous families, in fact, on several
different hosts than any other flowering plants. Related species of O. aegiptiaca cause especially heavy damages of melon in Central Asia, where
flowering plants not only reduce yield, but also encourage production of
toxins within melons that become commercially unusable. For example,
there are no reports of parasitism in soybean by any flowering plant, although O. crenata Forsk. is soybean parasite in a pot. However, pot assays
are valuable, for potential hosts can be identified on the bases of specificity
of domestic parasite strains that can be identified. In general, Orobanche
is the parasite of colder climates, and germination temperature is between
10 to 20 °C, alternately with temperatures of 5 °C. This can explain why
O. ramosa represents a problem in the river Nile valley in Sudan only in
winter, and the fact why O. cernua Loefl. attacks tobacco in India, and it
does not represent a problem in sunflower (Helianthus annuus) grown in
the same region during summer. Orobanche noticeably weaken roots of its
host. The longest dormancy of Orobanche seed in the soil was documented
in Bulgaria in 1956 due to severe Orobanche infection, in tobacco fields of
Tobacco Research Institute near Plovdiv, was planted a vineyard. In 1991
vineyards were removed and tobacco was sown again. Great number of O.
ramosa occurred probably out of seed that were dispersed during previous tobacco cropping in 1956. O. ramosa imported in California makes
a problem on tomato. Despite efforts to eradicate it, the parasite keeps
surviving. It is highly probable that parasite seed was imported by the
crop, by either infected plant or contaminated tomato seed. More recent of
tomato in Chile should be used as a warning that O. ramosa infection can
be expected wherever there is a convenient host.
Orobanche cernua is widely distributed in East Europe and Middle
East, with heavy invasions in South India and sporadical occurrences in
North Africa, China and East Europe. Its primary hosts are crops from
Solanaceae family and sunflower. Sunflower is the most important oil
plant in some parts of East Europe, and O. cernua is a major constraint
for production, especially in Bulgaria in which sunflower oil is a national
brend. Infected plants are stunted and have smaller heads and lower oil
quality. Between 1947 and 1950, Orobanche created a problem that in
Bulgaria became so serious that it threatened further sunflower existence.
Tobacco can be seriously damaged by O. cernua; however, tobacco was
not attacked in Bulgaria, even in regions near heavily infected sunflower
fields. In India in which tobacco is heavily damaged, situation is inverted
and sunflower was not attacked. It has been proved that O. cernua devel-
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Blagojević et al.
ops on hosts from family Solanaceae and that it will not attack sunflower.
Russian breeders studied O. cernua development for many years. Their
data should be studied and proved by new genetic methods (PCR). Given
the size of the area under sunflower, more awareness on this pathogen is
needed. Yet another of the species from Orobanche genus is O. crenata.
Main hosts of this species are ordinary beans, lentils, forage legumes, carrot, parsley, celery and etc.
The other two genus of Orobanchaceae family, Aeginetia and Christisonia, can be considered smaller problem on monocotyledonous plants.
In agro-ecological region of Serbia, broomrape on sunflower in greater
or lesser extent occurs almost annually and can cause significant damages. One of the most efficient and the most economical ways of control
of these parasitic flowering plants is certainly sowing of resistant hybrids.
For studies on hybrid resistance to broomrape it is very important to have
broomrape seed of good rate of emergence. Trifender is biological product
based Trichoderma asperellum. Broomrape rate of emergence is the lowest on medium with trifender; thus, the effect of this biological product for
seed germination should be studied in more detail (Maširević et al., 2011).
Orobanche cumana Wallr., as well as other parasitic plants from the
family Orobanchaceae, demand presence of chemical compounds from
the environment as stimulus for germination. In the study of Plakhine et
al. (2009) showed that seed germination of O. cumana. is improved due
to influence of synthetic nijmegen-1 strigolactone applied directly to dry
seed. Studies directed toward development of PCR methods for detection of seed abundance of two parasitic plants Phelipanche ramosa and
Orobanche cumana, as well as related species are used during harvest of
rapeseed and sunflower. The method is based upon design of the starting
probing. The method is based on the design of initial probing that is set for
each parasitic plant with determination of transcribed space sequences for
quantitative PCR determination. Together with the proposed DNA protocol, this diagnostic method allows a faster, high-throughput and accurate
assessment of contaminated rapeseed, without complex purification steps
and identification under a binocular microscope. TaqMan assay is highly
specific, since it is not possible to detect plant impurities that are present
in a given crops seed. The results of this test can be presented via the number of parasite seeds per kilogram of crops seed, which can contribute to
improved sales of crops seed (Rodriguez et al., 2010). It is known that a
new specific bioassays lead to the discovery of new classes of biologically
active compounds (Yoneyama, 2010).
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Biological characteristics of some parasitic flowering plants
Cuscuta L.
Cuscuta species, commonly known as dodder is among the best
known parasitic plants, and is one of the most invasive weeds in the world.
Species of Cuscuta, known as field dodder is among the best known parasitic plants, and it is one of the most invasive weeds in the world (Lowe
et al., 2001). Field dodders have wide spectrum of hosts, although they
favour less monocotyledonous species. Genus Cuscuta contains three
sub-genuses. Members of subgenus monogina are robust vines that attack
and destroy fruit trees, while the species in subgenus Cuscuta represents
a problem for hosts of the herbaceous plants, as well as subgenus Grammica. Infected plants weaken; vegetative luxuriance is reduced, as well
as their fertility (Koskela et al., 2001; Fathoulla and Duhoky, 2008). In
moderate climate, field dodder is maybe the most important parasitic weed
of legumes. C. campestris in alfalfa (Medicago sativa) is of special importance. Alfalfa and field dodder seed are alike by size, and by alfalfa sowing the parasites spreads with the host. The most efficient control measure
is sowing of pure seed. Due to bumpy surface of field dodder seed, it
retains, and cylindrical seed of alfalfa passes. Genus Cuscuta belongs to
the family Convolvulaceae, although some authors think that it belongs
to the other family (Cuscutaceae). Many species that are hardly recognizable and are able to parasite numerous shrubby and woody species belong
to this genus. Although the results of the mitochondrial genome analysis confirmed a link between the family Convolvulaceae (McNeal & DePamphilis, 2000), some studies also show that Cuscuta phylogenetically
belongs to the family Convolvulaceae (Stefanovic et al., 2002;. Stefanovic
& Olmstead, 2004).
The most widespread species in our country is Cuscuta campestris,
that is considered holoparasitic for it does not have pigments for photosynthesis. Performed assays showed that it contains chlorophyll (a or b),
during its whole vital cycle, although in much smaller quantities than other
green plants. Presence of this pigment varies depending on plant development stage and reaches maximum during flowering. In it are present
chloroplasts that function during whole plant life cycles that are able to
perform photosynthesis by chlorophyll, although to a lesser extent, which
forces it into heterophyl nutrition. Cuscuta campestris is extremely difficult to control, due to its well coated seeds, as well as its natural joining
in host-parasite association. Making part of ‘’seed bank’’, Cuscuta seed in
the soil maintains rate of emergence for long time, and it can survive at
least 10 years in the field and up to 50 years in dry warehouses, depending
77
Blagojević et al.
upon the species (Dawson et al., 1984). Chickpeas are very susceptible
to C. campestris. However, there are several efficient selective products
that are used in control of this parasite in chickpeas crops. After studies
of several genotypes of Israeli varieties that are resistant to C. campestris,
genotypes ICCV 95333 and Hazera 4 showed high resistance in more than
80% of the studied chickpeas (Goldwasser et al., 2012).
Seeds of C. campestris are different in size and usually germinate in
the following year, creating radicle rich in nutrients and a stem. Radicle
first penetrates slowly into the soil, but later it degenerates and decays so
that the plant loses all connection with land. The stem is able to grow up to
a month until it meets the host plant on which it fastens. It is in the form
of a thread, with varying looks, yellow-whitish in colour, with no leaves
and it is able to hold onto the host plant due to hooks, or papillae. The
flowers are white, small and produce many seeds. The most frequent host
plants of Cuscuta campestris are medicinal plants from family Fabaceae,
as well as sugar beet crop. Control of this parasite is performed primarily by preventive measures, in order to inhibit seed germination. If the
parasitic plant has already spread, herbicide application that acts on cell
division is efficient. Field dodder is certainly great problem in cultivation
of cranberry and other fruit trees shrubs (Sandler, 2010). With the aim of
field dodder control, treatment is made in alfalfa 1-3 trifoliate leaf stage,
or after first cutting with some of the following herbicides: imazethapyr,
clethodim, propyzamid, diquat and fluazifop-p-butyl (Konstantinović et
al., 2004). Use of Cuscuta species in control of invasive weed species is
a new approach that is being developed in China in last years (Yu et al.,
2011; Shen et al., 2011).
Conclusions
Even though 270 genera and 4400 species of flowering parasites are
parasites, only about 25 genera have negative impact to cultivated plants
and thus are considered pathogenic. Among them, two genera are the most
harmful - Orobanche (broomrape) and Cuscuta (field dodder). Parasitic
flowering plants are particularly harmful on legumes and crops belonging
to family Solanaceae, primarily genus Orobanche. It produces thousands
of tiny seeds that survive in the soil ‘’seed bank’’ that makes control very
difficult. However, as an integral part of every ecosystem that is compatible with its hosts, control is the only way for control of this parasite.
Knowledge of the complex biology of parasitic flowering plants requires
simultaneous studies of the host and parasitic flowering plant.
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Biological characteristics of some parasitic flowering plants
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