6 Striga Resistance in Cereal
6 Striga Resistance in Cereal
6 Striga Resistance in Cereal
StrigaResistanceinCerealCropsRecentProgressandFutureProspectsAReview
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Striga Resistance in Cereal Crops: Recent
Progress and Future Prospects. A Review
Maryam A. Dawud
Abstract- Production of cereal crops such as sorghum, maize, therefore these species are called obligate parasites
rice and millet is threatened by Striga hermonthica (Del.) Benth (Parker, 2009).
and Striga asiatica (L.) Kuntze in sub-Saharan Africa and India. The genus Striga consists of obligate
Varying levels of resistance have been identified and exploited
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hemiparasitic root parasites, some of which are serious
in the breeding programmes of several crops. Considerable
agricultural pests (Parker, 2009).They are a major biotic
efforts have been invested in breeding for Striga resistance in
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cereals and significant progress has been made in the constraint and a serious threat to subsistence cereal
development of improved selection methods. However, the crops (Pearl millet, finger millet, sorghum, maize and
level of protection achieved to date is incomplete especially for upland rice) grown in sub-Saharan Africa and India 39
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orphan crops such as pearl millet. Resistance is mainly ((Rispail et al., 2007; Teka, 2014). In Striga-prone
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also the development of alternative methods to control the 64% of the total cereal production area in West Africa
parasite. However, it is only a beginning that requires to be (Figure 1) (Gressel et al., 2004; Ejeta, 2007; Parker,
further exploited. This review presents an overview on recent 2012), and are continuing to expand. Infection of crops
advances in research on Striga in cereals and potential can result in grain yield losses, of 20-80% in Africa but
prospects using genomic tools as mentioned above with a
up to 100% in worst situations, and as consequence,
final aim of crop improvement.
have a significant negative impact on food security in
Keywords: striga spp., resistance, cereals, recent
these regions (Gurney, Press, & Scholes, 2002).
progress, potential prospects.
I. INTRODUCTION
P
arasitic plants are a major threat to today’s
agriculture and provide an intriguing case of
pathogenesis between species of relatively close
evolutionary ancestry. Almost all crop species are
potential hosts for parasitic plants, but severe disease
outbreaks are usually restricted to certain host–
pathogen combinations (Spallek et al., 2013). The
evolutionary strategy of exchanging autotrophy for
dependence on host plants (parasitism) may seem odd,
but it has proven to be evolutionarily successful for
several plant species. Plant parasitism has arisen at
least 12 times independently, generating more than
4000 parasitic dicotyledonous plant species (Westwood
et al., 2010). Although some parasitic plants are still
photosynthetically active (hemiparasitic), others are not,
and depend entirely on a host (holoparasitic). The
establishment of parasitism is essential for holoparasites
and several hemiparasites such as Striga spp., and
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Figure 1: Striga affects millions of smallholder farmers in sub-Saharan Africa(Mignouna et al., 2013)
Global Journal of Science Frontier Research ( D ) Volume XVII
Infested area and level are likely to increase in the presence of partial quantitative resistance to S.
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the near future because of continued increase in cereal hermonthica in wild pearl millet relatives originating from
monoculture in some parts of Africa that has led to Africa.. Kountche (2013) also stressed that, progress in
reduced soil fertility coupled with high moisture stress, genetic, genomic and physiological characterization of
and the weed has consequently been described as an Striga resistance mechanisms is essential for the
indicator of low soil fertility (Oswald, 2005;Teka, 2014). sustained improvement of pearl millet, which is the least
Agronomic control of Striga aimed at limiting Striga seed studied major cereal crop cultivated in Africa.
production, but as each Striga plant sets tens of This paper presents the latest information on
thousands of seeds that can live for so many years, breeding for resistance to Striga in cereal crops and
control appears very difficult (Kountche, 2013). Genetic future prospects.
control of Striga, where possible, is widely considered to
be the most practical and economically feasible method II. Striga Biology and Life Cycle
for long-term control of Striga (Ejeta, 2007; Hearne, ‘Striga’ is the Latin word for ‘witch’. Witchweed,
2009; Yoder & Scholes, 2010). Mukarram (Shuwa Arab), Maakasha or wuta wuta
Many scientists (Haussmann et al., 2001; (Hausa) and other common names for Striga often refer
Omanya et al., 2004; Gurney et al., 2003; Cissoko et al., to the word ‘witch’, fire or killer presumably because
2011; Jamil et al., 2011) in the past have made intense plants diseased by Striga display stunted growth and an
investigation, to characterize the mechanisms and overall drought-like phenotype long before Striga plants
inheritance of resistance to Striga spp. in some major appear. Striga species are annual plants and most of
cereal crops such as sorghum, rice, and maize. This their life cycle occurs underground (figure 2) (Spallek et
was followed by the development of molecular markers al., 2013). Striga plants are highly reproductive (10 000
associated with Striga resistance and quantitative trait to 200 000 seeds) and can remain dormant in the soil
loci (QTL) in sorghum and their introgression into elite for more than 20 years before germination (Parker &
varieties (Haussmann et al., 2004;Gurney et al., 2006; Riches, 1993). Germination is linked to the presence of
Satish et al., 2012; Mutengwa et al., 2005; Rispail et al., a nearby host, because the endosperm of Striga seeds
2007). However, despite these efforts, precise, validated can sustain it survival only for the first 3–7 days (Berner
information on the inheritance of resistance to Striga is et al., 1995). Within that time, Striga must successfully
still lacking in cultivated pearl millet (Kountche, 2013). establish a parasitic relationship with the host plant or
Some scientists report the presence of resistance to otherwise die. This aspect was successfully exploited
Striga in cultivated pearl millet (Ramaiah, 1987), but during S. asiatica eradication programme in the USA,
these reports were questioned by other authors (Chisi & when ‘suicide germination’ was induced by fuming
Esele, 1997). So far, Wilson et al. (2000, 2004) reported farmland with ethylene to trigger Striga germination in
the absence of host plants (Parker, 2009).These Striga 1999; Dorr, 1997). This allows the direct transfer of
seeds germinates only in response to specific water, carbohydrates and nutrients from the host plant
chemicals, most commonly strigolactones, which are to the parasite, drastically reducing host plant growth
apocarotenoid signaling molecules (Matusova et al., and yield (Parker & Riches, 1993; Van, 2006).
2005). The germination of Striga depends on the Subsequently, Striga grows upwards and adventitious
perception of germination stimulants released by host roots are produced, emerges above the ground and
roots. In order to be responsive to germination flowers to produce seeds (Spallek et al., 2013).
stimulants, Striga seeds must go through a phase of In many cases, S. hermonthica seeds collected
moisture and high temperatures for 7–14 days, called from one cereal host can infect other cereal species,
‘conditioning’. If, during that time, no germination although there is evidence for some interspecies
stimulant is perceived, Striga seeds fall into a secondary specificity, particularly with respect to the reciprocal
dormancy. Strigolactones are certainly the best studied infectivity of populations of S. hermonthica collected
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and extremely potent inducers of Striga germination from sorghum and pearl millet (Vasudeva & Musselman,
(Spallek et al., 2013). The signals are then released by 1987). Perhaps, genetic variation is likely to be
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the host plant roots into the rhizosphere (Bouwmeester maintained within populations (ecotypes) from
et al., 2003;Yoneyama et al., 2010; Xie et al., 2010). The generation to generation, especially in S. hermonthica
concentration of stimulant required to initiate Striga seed (Bharatha et al., 1990). More recently, the presence of 41
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germination ranges from 10-10 to 10-16 mole m-3 genetic variation for host range specificity within S.
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host xylem–xylem connections (Figure 2) (Albrecht et al.,
Figure 2: Stages in Strigalife-cycle and its interaction with the host plant(Ejeta & Butler, 1993)
III. Striga Control Methods been developed (Atera et al., 2011). Despite efforts
made to control the Striga problem, it has persisted and
Research aimed at Striga control has been carried increased in magnitude prompting to research aimed at
for a long time and a wide range of technologies have preventing infestation. Many potential Striga control
methods have been applied, ranging from agricultural control, and a return to investment, and an unwillingness
practices to biological control (Joel, 2000). According to to make the long-term investments (Joel et al., 2007).
Haussmann et al.(2000) Striga control strategies can be Considering the challenges to a successful control of
broadly classified into three major categories that have the parasitic weed so far, it is generally believed that no
different impacts on a Striga population: (1) reduction of single method of control can provide an effective and
the Striga seed bank; (2) limitation of Striga seed economically feasible solution. Therefore, the most
production; and (3) reduction/prevention of Striga seed practicable, comprehensive and sustainable way to deal
dissemination to uninfested fields. Also, Strategies may with this parasitic weed is integrated control approach
be directed to the alternative management options of which is essential, ideal and useful to small-scale
Striga control, containment, or eradication (Ejeta & farmers, in order to achieve sustainable crop production
Gressel, 2007). Although, control of Striga could be slow (Teka, 2014; Ejeta, 2007)). Therefore, control strategies
but is feasible. The severity of Striga damage and should be geared towards individual cropping systems,
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infestation can be reduced with well-managed practices local needs and preferences to help adapt and optimize
and measures that fit the local knowledge, economy, as control strategies to different agro-ecosystems. Oswald
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well as labor capacities, and practiced for several (2005) suggested first containment, sanitation as a
seasons. Four independent Striga control approaches measure to prevent Striga damage and finally
42 that have been widely investigated and developed have eradication, as a means to eradicate the soil Striga seed
been outlined by Ejeta and Gressel (2007); cultural, bank. According to FAO(2016) and Khan et al.(2008) the
Issue III Version I
chemical, genetic, and biological options. Some of “push pull” system of integrated pest management
these control options aim to improve soil fertility, through inhibit Striga growth and does not need high levels of
the use of organic and inorganic fertilizers, while others external inputs. Also, farmers have adapted “push pull”
directly affect the parasite (Rector, 2009). So far the to allow intercropping with beans and report that their
various control options available to farmers include; the maize yields have increased three to four times. In
use of cultural and mechanical practices such as hand- northern Nigeria, some farmers control Striga by
pulling, crop rotation, trap-cropping, intercropping, applying organic and inorganic fertilizer and crop
Global Journal of Science Frontier Research ( D ) Volume XVII
appropriate improvement of soil fertility, soil and water rotation (Dugje et al., 2006). Ibrahim et al. (2014) also
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management, tillage and planting methods (Hess & suggested the use of cover crops such as Mucuna spp.
Dodo, 2004; Jamil et al., 2011) biological control using as an intercrop to reduce Striga infestation. The potential
the insect Smicronix spp or pathogenic fungus Fusarium use of sesame as a trap-crop in integrated control of
oxysporum as a mycoherbicide (Marley et al., 2005; Striga in pearl millet was reported by Hess & Dodo
Zahran et al., 2008; Rebeka et al., 2013) application of (2004). Also, Midega et al. (2013) reported significant
chemicals using pre-emergence and post emergence decrease in Striga count when desmodium was used as
herbicides (Kanampiu et al., 2003) and host plant an intercrop to control Striga in maize. Integrated Striga
resistance (sorghum, rice and maize) (Parker & Riches, management package combining a mycoherbicide
1993; Haussmann et al., 2000; Gurney et al., based on F. oxysporum isolate and host plant resistance
2006;Hearne, 2009; Teka, 2014). The fact that has been demonstrated on farmers’ fields as effective
symptoms of Striga damage on the host appears before Striga control approach (Yonli et al., 2012; Teshome,
Striga emerge above the ground illustrates how 2013; Teka, 2014). All these facts demonstrate the need
ineffective the control of the parasite by hand weeding for integrated Striga control as an effective tool in
or application of herbicide is likely to be. Therefore, addition, reduce the environmental impact of individual
control methods that affect Striga germination and control strategy. It has generally been accepted that,
attachment to the host are expected to be more Striga can be controlled if a wide range of individual
effective because they prevent the host from Striga control methods are brought together as a program of
parasitism. Nevertheless, former techniques are integrated Striga control (ISC), to serve a range of bio-
important because they could avoid the reproduction of physical and socio-economic environments (Ellis-Jones
Striga thereby reducing the seed bank. Elzein et al. et al., 2004; Douthwaite et al., 2007; Harker &
(2010) reported Fusarium oxysporum is highly effective O’Donovan, 2013). According to Atera et al. (2011) the
in hindering germination, growth and development of major objective of ISC is to reduce Striga densities in the
Striga. Also, the fodder crop legume, Desmodium soil thereby avoiding new Striga plants from emerging in
uncinatum is highly effective in controlling Striga as the subsequent seasons. Moreover, integrating genetic
reported by Khan et al.(2008), as it attract the parasite resistance with other technologies is the smartest option
thereby preventing the host from Striga attack. In possible both for effectiveness of control as well as for
general, only a few of these control measures have been increasing durability of resistance genes (Ejeta, 2007;
widely adopted or commercialized. Low adoption of the Cissoko et al., 2011). In recent years, efforts have been
control practices are as a result of limited knowledge of undertaken to elucidate the molecular characterization
the problem, its biology, the lack of labor or resources to of the host plant – parasite interaction and host
make the needed investment, an uncertainty of potential resistance through expression analysis of the genes,
proteins and metabolites involved in these processes experiments need to be tested in the field, because
(Rispail et al., 2007; Aly, 2012). Recent discovery of a laboratory environment is different from field
new class of plant hormones, strigolactones by environment. Recently, a number of genes or
Yoneyama et al. (2010) not only controlled branching chromosomal regions that control quantitative traits,
but also play a role in attracting Arbuscular mycorrhizal quantitative trait loci (QTL), associated with resistance to
fungi (AMF).Strigolactones are certainly the best studied Striga spp. in sorghum (Haussmann et al., 2004; Satish
and extremely potent inducers of Striga germination (Xie et al., 2012), and rice have been reported (Gurney et al.,
et al., 2010; Kohlen et al., 2011). 2006; Kaewchumnong & Price, 2008). As a result, QTLs
An RNA interference (RNAi) technology was have been refined to introgress Striga resistance into
recently investigated as a genetic tool for enhancing farmer-preferred sorghum varieties in most parts of
host resistance against parasitic weeds (Yoder et al., African countries (Grenier et al., 2007). Marker assisted-
2009). The development of herbicide-resistant crops is selection techniques for parasitic plant resistance can
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an alternative approach to the control of parasitic weeds be used to rapidly accumulate several resistance genes
(Gressel, 2009). However, these approaches use (Rispail et al., 2007). However, marker-assisted
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genetically modified organisms and may thus not be backcrossing (MABC) has certain limits for introgressing
easily adopted by farmers and (Kountche, 2013), in a quantitative trait (Kountche, 2013). Since markers to
addition, may be associated with problems in the field be used in MABC are usually identified in biparental 431
(gene flow, coexistence with local varieties). The mapping populations, this becomes a limitation in
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Considerable efforts have been invested in
resistance(Bernardo & Charcosset, 2006). However, the
breeding for Striga resistance in cereals and significant
most important point to note in molecular breeding for
progress has been made in the development of
resistance to Striga is the identification of strong
improved selection methods. Haussmann et al., (2000)
associations between genetic markers and the genes
reported an improved field testing method for Striga
that determine resistance to the parasite.
resistance. More recently, Kountche et al. (2013) used
Because of the ability of Striga spp., particularly
phenotypic recurrent selection to breed for Striga
S. hermonthica, to break down resistance (Rich & Ejeta,
resistance under field conditions and this resulted in
2008), deliberate stacking of quantitative (polygenic)
significant improvement in Striga resistance in cultivated
resistance in addition to the qualitative (monogenic)
pearl millet and the development of the first pearl millet
resistance in the cultivars to be used reduces the
Striga-resistant experimental varieties. However, multi-
likelihood of resistance breakdown. Gene stacking is of
location field screening for Striga resistance resulted in
upmost importance for durability because multiple
significant genotype ×environment (G×E) interactions
mutations would have to accumulate in the parasite
for Striga resistance traits in sorghum, maize and pearl
population to overcome resistance genes in the host
millet trials (Haussmann et al., 2001; Badu-Apraku et al.,
(Rich & Ejeta, 2008). Kountche et al. (2013) reports that,
2010). These results suggest that there is need to select
the use of genetically different Striga-resistant open-
for specific adaptation in Striga resistance breeding,
pollinated cultivars, with different resistance alleles,
particularly in the case of contrasting environments
could be a practical alternative to stability of resistance
where different putative Striga ecotypes may exist. The
over time.
use of laboratory-based assays, on the other hand, has
enabled further insights into the interactive biological V. Research Achievements
processes between Striga and the roots of host plants
during each individual stage of the parasitic process Significant advances have been made on Striga
(Ejeta, 2007). The power of the physiology-based control research in Africa from 1940s onwards
breeding approach is that it pushes the limit of what (Andrews, 1947; Ejeta, 2007) and, in the last 20 years
would traditionally be considered good source material these efforts have been increased and considerable
for resistance to the parasitic weed (Kountche, 2013). resources have been invested in developing control
Physiology-based approaches have also threw more options (Oswald, 2005; Khan et al., 2010; Midega et al.,
light on the specific mechanisms of resistance 2013). Several organizations have been involved in
associated with each source of host genotype (Ejeta & conducting Striga control research in Africa. These
Butler, 1993; Gurney et al., 2006). However, laboratory includes; International Maize and Wheat Improvement
Centre (CIMMYT) (Odhiambo & Ransom, 1993)); sequencing technology (Yoshida et al., 2010). For
International Centre of Insect Physiology and Ecology example, comparative studies on repetitive regions in
(ICIPE) (Khan et al., 2008); International Crops Research five Striga species generated a total of about 2200
Institute for the Semi-Arid-Tropics (ICRISAT) Sanger sequence reads and about 10 000 454 reads
(Haussmann et al., 2001); Integrated soil fertility (Estep et al., 2012). Partially assembled and identified
management program in sub-Saharan Arica by IITA, repeats were most similar to the most closely related
IFDC and IPNI (Vanlauwe et al., 2015); African plant species. Overall, the authors came to the
Agricultural Technology Foundation (AATF) and conclusion that the analysed Striga genomes have a
International Institute of Tropical Agriculture (IITA) rather typically complex angiosperm genome. Estimated
(Manyong, 2008). Other institutions from advanced haploid genome sizes range from 615 Mb for S. asiatica
countries mostly from Europe (The UK and The and 1425 Mb for S. hermonthica suggesting several
Netherlands), USA and Canada have also been involved polyploidization events.
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in conducting research on Striga (Andersson & No evidence of large transfers of repetitive DNA
Halvarsson, 2011). Recently, a four-year project regions from the hostgenomes was observed, which is
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Achieving sustainable Striga control for poor farmers in in contrast with the observed HGT events between
Africa (April 2011-March 2015) reported by Oluoch et monocot genes and S. hermonthica (Yoshida,et al.,
44 al.(2014), also known as the Integrated Striga 2010), and favours the hypothesis that HGT events
Management Project (ISMA), was conducted to improve originate from mRNA species rather than from large
Issue III Version I
Ahmadu Bello University, Nigeria, Bauchi State psu.edu/) (Westwood et al., 2012), genetic resistance
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Agriculture Development Programme (BSADP), AATF) based on silencing of a target gene in the host plant is
and local project sites to assure end users’ access to now feasible (Yoder et al., 2009).
technical information, technologies, and experience. Nevertheless, there is still a need for further
More than 10 herbicide and Striga resistant maize research into the mechanisms involved in the
hybrids and OPVs have been developed and promising translocation and regulation of the macromolecules
materials have been identified for further testing and involved in host- parasite interactions (Aly, 2012).
potential release in the two countries. These institutions Moreover, comparative genomics can point to
have recommended control options to farmers in Nigeria important resistance genes and signaling pathways in
geared towards reducing infestation and damage. The pearl millet as they were discovered in other Striga- host
options include: the use of resistant crop varieties, cereal crops (Michelmore, 2000; Rispail et al., 2007).
intercropping of cereals and legumes, crop rotation, use Alignment of the high-density pearl millet genetic map
of trap crops that stimulate suicidal germination such as currently under development will thus enable
desmodium, and application of manure and nitrogenous exploitation of comparable grass resources for the
fertilizer. identification of potential Striga resistance genes in pearl
Research on the parasitic weed, have been millet (Devos & Gale, 2000; Kountche, 2013).
going on for so long that it would be wrong to suggest
Next-generation sequencing technology has led
that there has been little progress in their control. From
to an increase in available transcriptional data for S.
the aforementioned studies, dedicated work leading to
hermonthica and related species. For example, Wickett
useful Striga control strategies have been done on at
et al.(2011) analysed sequence data obtained from
least local basis.
Illumina short reads of mRNA isolated from above-
VI. Next Generation Striga Research ground tissue of three Orobanchaceae species: the
facultative hemiparasite T. versicolor, S. hermonthica
A thorough knowledge of the molecular bases and Phelipanche aegyptiaca (pers.) Pomel. The
of resistance to Striga is essential to provide the expression of photosynthesis-related genes was much
fundamental information necessary to drive not only lower in S. hermonthica than in Triphysaria, and no
crop improvement but also the development of expression of these genes was detected in Phelipanche.
alternative control methods. The study also revealed that chlorophyll a synthesis
In recent years, efforts have been undertaken to gene expression was conserved and detectable in all
elucidate the molecular events underlying Striga three species, even in the non photosynthetically active
infections using next generation and conventional Ph. aegyptiaca.
Next-generation sequencing technology will is rooted in the high complexity of the interaction and
almost certainly provide detailed transcriptional the nature of the parasite. The detection of partial
information for Striga at different stages of infection and resistance within genotypes of some crop oriented
on different hosts, and will allow the simultaneous further development of control methods toward genetic
detection of host and pathogen transcriptomes. So far, crop improvement. However, the multigenic and
host transcriptome data are mainly based on microarray quantitative system generally controlling the resistance
studies or similar methods. Hiraoka et al. (2009) used a dramatically slows down breeding. It is now evident that
suppression subtractive hybridization strategy of mRNA efficient control of the parasite requires a more
isolated from Lotus japonicus to investigate differences comprehensive understanding of the molecular bases of
when infected with S. hermonthica (resistant) or Ph. the interaction and its transfer to breeders. The few
aegyptiaca. studies targeting the analysis of gene expression and
The accumulation of cytotoxic material is also accumulation of proteins and metabolites start to reveal
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probably the cause of nonhost resistance to S. the molecular dialogue involved in resistance. However,
hermonthica in Tripsacum dactyloides, a wild relative of it is only a beginning that requires to be further
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maize. In contrast with Z. mays, haustoria formation is exploited. Application of some of these biotechnological
impaired on T. dactyloides plants by an unknown factor. tools has already been initiated to tackle plant parasite
This factor is also able to suppress haustoria formation problems such as MAS or the ‘omic’ technology, but to 45
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on Z. mays, when Striga plants are attached to T. develop resistant crops the inclusion of other tools such
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encoding pathogenesis-related (PR) proteins, WRKY genes to improve resistance in crops, which will need to
transcription factors and pleiotropic ABC transporters, be validated through functional analysis. In addition, the
whereas the compatible (susceptible) interaction was better understanding of the interaction and the parasite
characterized by large-scale down-regulation of genes biology gained by these molecular methods may also
associated with growth regulation, metabolism, allow the development of new methods of control.
biogenesis of cellular components and cell division. Although much work remains to be done, the different
Several genes coding for nutrient transporters, enzymes approaches presented in this review should, in the near
involved in amino acid metabolism, were up-regulated future, provide solutions to the problems caused by
at the same time in the susceptible rice cultivar. parasitic plants.
Overall, these data, although sometimes very
difficult to compare, draw a common picture, in which References Références Referencias
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