Abstract
This chapter provides an overview on the biology of the parasitic weeds of the genus Striga, specifically S. asiatica and S. hermonthica, and their impact on three cereal staples of sub-Saharan Africa, maize, rice and sorghum. Host plant resistance to Striga mitigates the yield losses to these crops. Improvement of Striga resistance in these three crops is discussed including the possibility of expanding resistance sources through mutagenesis.
You have full access to this open access chapter, Download chapter PDF
Similar content being viewed by others
Keywords
Striga and Its Parasitic Relationship with Cereals
Through their evolutionary course, some plants have lost their autotrophic nature and depend on other plants to provide them with the water and nutrients they require to complete their life cycle. These parasitic plants account for approximately 1% of angiosperms, totalling over 4000 species distributed in over 30 families (Nickrent 2018). Most parasitic plants are curious members of natural ecologies rather than agricultural pests. A few, like sandalwood, are even valuable crops themselves. Some, however, have adapted to crop hosts and have therefore become weeds. Striga is a genus name in the family Orobancaceae which contains 1725 parasitic plant species (Nickrent 2018). Striga itself includes approximately 40 species, all hemiparasitic, meaning that they have retained some photosynthetic capacity, but all obligate parasites, requiring a host plant to survive through maturity. Most Striga species parasitize grass hosts with S. gesnerioides, a parasitic weed in cowpea, a notable exception. The name Striga is the Latin word for witch. Striga are therefore commonly known as witchweeds in English with similar common names in the languages of many sub-Saharan African peoples that inhabit their native range. The name is descriptive of the syndrome cereals display under Striga infestation. Even before the weed emerges and transforms a grain field into a sea of red or purple flowers, the crop appears to be under a spell that robs it of its verdancy. The most notorious Striga species are S. asiatica and S. hermonthica and it is to these which we refer throughout this book as Striga. Striga causes an estimated seven billion USD in crop productivity losses annually across sub-Saharan Africa (Yacoubou et al. 2021). Striga are in many agroecologies the primary biological constraints to maize, rice and sorghum production. There are few control options among these crops. These include host plant genetic components that mitigate the degree of Striga infestation (resistance) and impact of infestation on crop productivity (tolerance). Host plant resistance and tolerance are considered vital components of Striga management strategies, but unfortunately sources are rare and largely uncharacterized among these staple grain crops (Rich 2020). Yield losses to Striga are concentrated among the subsistence farms where agricultural inputs that can reduce their impact (e.g., irrigation, fertilizer and even improved cultivars) are rarely used. It is with view to these farmers that this mutagenesis project was undertaken.
In order for the parasite to succeed on its host, it must cue its development to a series of vulnerabilities manifested by the cereal during its growing season. These are described in more detail in Chapters “Physical Mutagenesis in Cereal Crops”–“An Agar-Based Method for Determining Mechanisms of Striga Resistance in Sorghum” and elsewhere (see Rich 2020), but briefly involve germinating in response to chemical stimulants (strigolactones) exuded by the host seedling root. Next, the Striga radicle tip must form a haustorium (organ of attachment and acquisition) at or very near an actively growing host in response to 2,6-dimethoxybenzoquinone (DMBQ) and other by-products of secondary cell wall formation. The haustorium must then attach to the host root and penetrate the epidermis, cortex, endodermis and xylem elements, all the while evading any host defences that could halt its progression. Further haustorial development must then occur until a functional vascular union is achieved with its host, ensuring a sustained flow of water and nutrients to support Striga shoot development and sufficient growth to the point of emergence, flowering and seed production. A healthy S. hermonthica plant can produce in excess of 100,000 seeds and these seeds can remain viable for a decade or longer.
Resistance traits can be anything that interferes with establishment of this parasitic relationship, rendering a host less compatible to Striga infection at any or multiple points of this process such that the number or vigor of successful parasites is reduced relative to that on a susceptible, or more compatible host. Reducing the number of successful parasites protects both the current and future crops. Beyond the effects of resource theft, Striga is notorious for further negative effects on host plant fitness, things like increased root growth at the expense of shoot growth, chlorosis and leaf senescence, which in crop plants translates to severe or even total reductions in grain yield. Tolerance traits affect a host’s ability to be less sensitive to these peculiar toxic effects of Striga infestation and thereby sustain grain production in comparable amounts to uninfested plots.
Striga on Maize
Although maize (Zea mays) is an introduction from the Americas, it is today the major cereal crop in both area under cultivation and grain production in Africa (Rich and Ejeta 2008). Striga is a major biological constraint to maize cultivation across most areas of sub-Saharan Africa (SSA) and thereby reduces food security of millions of farmers and those that depend on the grain they produce (Yacoubou et al. 2021). There are limited control options and most of these are not readily available to subsistence farmers, by far the most numerous in Striga endemic areas. Integrated approaches employing both resistant varieties along with Striga management practices are generally more effective than singular control methods, but again, too costly or unavailable to most maize farmers in SSA (Rich 2020; Yacoubou et al. 2021). Sources of genetic resistance to Striga are rare and come largely from maize’s wild relatives, Tripsicum dactyloides and Zea diploperennis (Gurney et al. 2003; Amusan et al. 2008). Other sources include landraces, inbred lines, open pollinated varieties and some hybrids (Yacoubou et al. 2021). Tolerance, (reduced impact of Striga infestation on yield) is used more in maize than genetic resistance (host plant factors that reduce Striga infestation) because the former is more widely available (Yacoubou et al. 2021). However, tolerance does little to control the spread of Striga among maize production areas and pest populations can quickly overwhelm these lands to the point where they are no longer suitable for maize cultivation (Yacoubou et al. 2021). Known resistance mechanisms in maize include low Striga germination stimulant activity of root exudates (Gurney et al. 2003; Adetimirin et al. 2000; Karaya et al. 2012), low haustorial induction (Gurney et al. 2003; Mutinda et al. 2018), reduced attachment due to reduced host root branching (Amusan et al. 2008), reduced number of successful penetrations (Gurney et al. 2003; Amusan et al. 2011) and escape through early maturity (Oswald and Ransom 2004). The genetic basis underlying these resistance mechanisms remains poorly understood. No known genes specifically controlling resistance/susceptibility have been identified and therefore markers for Striga incompatible alleles do not yet exist (Yacoubou et al. 2021).
Striga on Rice
Although one species of rice (Oryza glaberrima) was domesticated in West Africa nearly 3000 years ago, the predominant species cultivated across sub-Saharan Africa is now Asian rice (O. sativa) introduced through East Africa from India 500 years ago and is today the second most important cereal on the Continent (Zenna et al. 2017). A group of rice varieties called NERICA (New Rice for Africa) developed at the Africa Rice Centre in East Africa from crosses between the native and introduced rice species are promising sources of Striga resistance (Rodenburg et al. 2017). Genomic regions in rice associated with Striga resistance have been reported. One of the progenitors of the mapping population used to identify quantitative trait loci (QTL) for Striga resistance was a line that showed a strong incompatible reaction to S. hermonthica. Parasites were unable to establish vascular connections with the rice host (Gurney et al. 2006). From testing the mapping population under Striga infestation, four QTL with major effects on resistance to S. hermonthica were identified. Expression profiling was used to find three candidate genes coding for uncharacterized proteins within one of the major QTL associated with resistance (Swarbrick et al. 2008). Quantitative trait loci with major effects on tolerance to S. hermonthica have also been reported in rice (Kaewchumnong and Price 2008). Mechanisms of low Striga germination stimulant activity and incompatibility were characterized among rice cultivars with field resistance to both S. asiatica and S. hermonthica (Samejima et al. 2016; Rodenburg et al. 2017). In one of these, a gene involving regulation of salicylic acid and jasmonic acid defense signaling pathways was found to condition the resistance (Mutuku et al. 2015).
Striga on Sorghum
Sorghum was domesticated in the same parts of Africa where Striga is believed to have originated (Rich and Ejeta 2008). It is perhaps because the two species share a common geological origin that Striga resistance in sorghum is better defined than in maize and rice.
In sorghum, low Striga germination stimulant activity is a useful source of resistance. Inheritance of this trait is through recessive alleles (lgs1) at a locus named LOW GERMINATION STIMULANT1 (Gobena et al. 2017). Sorghum varieties homozygous for lgs1 generally support fewer Striga plants relative to susceptible varieties. The LGS1 gene codes for a sulfotransferase unique to sorghum that controls the stereochemistry of the strigolactones during the final step of their biosynthesis (Yoda et al. 2021). That stereochemistry determines the Striga germination stimulant activity of the strigolactones that dominate the sorghum root exudate (Gobena et al. 2017). LOW GERMINATION STIMULANT1 is currently the only known Striga resistance gene in any cereal.
Exudation of germination inhibitors is a possible Striga resistance trait in sorghum, although the chemical identity of these inhibitors remains largely unknown (Weerasuriya et al. 1993; Rich et al. 2004). Reduced haustorial inducing capacity of sorghum root exudates is another possible Striga resistance trait in sorghum. Complete lack of haustorial initiation factors released by growing roots is unlikely, given that DMBQ is a by-product of host root growth through elongation. Certain sorghum lignin mutations called brown midrib12 (bmr12) specifically reduce syringyl components of secondary cell wall lignin (Saluja et al., 2021). These syringyl lignin subunits are direct precursors to DMBQ (Cui et al. 2018). A preliminary test of haustorial inducing capacity of sorghum bmr12 mutants with S. hermonthica showed 20% fewer haustoria formed near the roots of these mutants in agar than occurred in the presence of wildtype sorghum roots (Rich 2018). Whether bmr12 sorghum is less parasitized in a soil environment remains to be tested. We have also observed lower haustorial initiation capacity among certain wild sorghum accessions (Rich et al. 2004).
Root characteristics like decreased branches may result in fewer Striga attachments through avoidance of potential parasites. We have observed in our various co-culture laboratory methods that Striga are more likely to attach to and successfully penetrate thinner root branches than on the primary roots of sorghum seedlings. The altered lignin mutation bmr12 also causes root architectural changes resulting in fewer branches in the upper soil profile with respect to wildtype (Saluja et al. 2021). Several other QTLs have been identified in sorghum that control root architecture (Parra-Londono et al. 2018) and certain alleles that specifically condition fewer root branches in the upper soil profiles may therefore contribute to Striga resistance through avoidance.
Sorghum has a reputation for producing allelopathic chemicals like sorgoleone produced in its root hairs (Głąb et al. 2017). Sorgoleone is a potent phytotoxin, inhibiting multiple vital processes impacting photosynthetic, root and mitochondrial functions (Dayan 2006). Phytotoxicity toward Striga has not been specifically studied. If sorgoleone or the other allelopathic compounds present in sorghum root exudates have an antibiotic effect on Striga, they would likely protect it at the pre-attachment phases of the life cycle. These and other components of sorghum root exudates might also act indirectly by influencing the microflora of the rhizosphere favoring Striga-suppressive rhizobacterial or mychorrhizal species (Schlemper et al. 2017).
A number of post-attachment resistance reactions have been described in sorghum that stops the parasite before vascular connections are established. One of these is an apparent hypersensitive response that shows reddening and necrosis in host root epidermal and cortical cells surrounding the attachment site, generally isolating the invading tissues and blocking parasite establishment. The response was described in derivatives from wild sorghum (S. bicolor × S. b. verticilliflorum) challenged with S. asiatica in laboratory co-culture and is inherited through dominant alleles at two loci named Hrs1 and Hrs2 (Mohamed et al. 2010). This defence response appears similar to the hypersensitive response characterized in cowpea against S. gesnerioides and may be triggered by as yet unidentified effectors from the parasite (Li and Timko 2009). Other reactions generally described as “mechanical barriers” have been reported in resistant sorghums upon attachment of S. asiatica expressed in the cortex and endodermis that prevent invading parasite tissue from reaching the vasculature (Maiti et al. 1984). We have used the term incompatibility to indicate the collective post-attachment resistance responses that do not have obvious host-tissue necrosis (Pérez-Vich et al. 2013). These may include several mechanisms controlled by multiple loci. The overall effect is to arrest or reduce the rate of successful parasitic events. In sorghum infected with Striga, these are usually not 100% protective, that is, some parasites on resistant varieties usually do manage to emerge and set seed, but the frequency of these events is reduced relative to the numbers of successful parasites on susceptible varieties. Incompatibility may be expressed in the cortex, at the endodermis or even after penetration of xylem vessels. Attached Striga in these instances are slow to develop and often die before reaching maturity. Incompatible reactions are expressed in host tissues as extra thickening of the endodermis and deposition of phenolic compounds at the interface with haustorial cells or even occlusion of vessels where the parasite initially breached its xylem elements (Maiti et al. 1984; Arnaud et al. 1999; Amusan et al. 2011; Mbuvi et al. 2017). The haustoria of Striga infecting incompatible sorghum often appears diminished relative to those of successful parasitic events. These symptoms may represent instances of active defence responses triggered by the parasite or simply a constitutively unsupportive cellular environment, perhaps lacking key metabolites preferred by the parasite to establish and grow. Unfortunately, none of these post-attachment reactions in sorghum to Striga have been so precisely characterized and exploited in resistance breeding as lgs1, and markers specific to only lgs1 currently exist.
Potential Contribution of Mutagenesis to Improved Striga Resistance
Multiple resistance traits, even those that render a plant slightly incompatible with Striga establishment, combined in a crop genotype are more sustainable than individual resistant traits since a parasite population would need to accumulate multiple virulence mutations to overcome them. Tolerance too is ideally used in combination with resistance for long-term durable protection. The challenge of deploying these host characters in a sustainable combination is that they are rare, almost never singularly effective (there are no credible reports of Striga immune varieties in these crops) and their genetic basis is poorly understood. Adding to these fundamental limitations for the use of host resistance/tolerance, access to Striga resistant varieties and inputs that extend their effectiveness by the neediest farmers is extremely limited.
It is in the context of these great challenges that this CRP offers a contribution. We wanted to create through mutagenesis more genetic variants that offer some degree of Striga resistance. With view specifically to farmer acceptance of any new resistant varieties that might result from this endeavour, each participating Member State chose a crop variety popular among subsistence farmers with several desirable qualities, but lacking Striga resistance, in which to conduct the mutation breeding. Since very few genes are known among the target crops that control Striga resistance, a process that caused genome wide changes seemed worth trying. The goal was to identify among the mutagenized lineages Striga resistant progeny in farmer-preferred varieties. Useful gained resistance should come as an attribute without yield costs or loss of other desirable characteristics. The resulting germplasm would then have added value as a cultivar itself, at least as a demonstration that a favourite genotype can be genetically protected against the ills of Striga. More appropriately in terms of sustainability, the germplasm would serve as starting material for further resistance improvements based on the introgression of other known Striga resistance alleles from crosses with donor sources or through gene editing. The fruit of this gained resistance would be even greater if the underlying mutations that caused the improved Striga resistance can be identified through genomic analysis and thereby become new targets for natural allele mining or gene editing.
References
Adetimirin VO, Kim SK, Aken’Ova ME (2000) Expression of mature plant resistance to Striga hermonthica in maize. Euphytica 115:149–158
Amusan IO, Rich PJ, Menkir A, Housley T, Ejeta G (2008) Resistance to Striga hermonthica in a maize inbred line derived from Zea diploperennis. New Phytol 178:157–166
Amusan IO, Rich PJ, Housley T, Ejeta G (2011) An in vitro method for identifying postattachment Striga resistance in maize and sorghum. Agron J 103:1472–1478
Arnaud MC, Véronési C, Thalouarn P (1999) Physiology and histology of resistance to Striga hermonthica in Sorghum bicolor var Framida. Functional Plant Biol 26:63–70
Cui S, Wada S, Tobimatsu Y, Takeda Y, Saucet SB, Takano T, Umezawa T, Shirasu K, Yoshida S (2018) Host lignin composition affects haustorium induction in the parasitic plants Phtheirospermum japonicum and Striga hermonthica. New Phytol 218:710–723
Dayan FE (2006) Factors modulating the levels of the allelochemical sorgoleone in Sorghum bicolor. Planta 224:339–46
Głąb L, Sowiński J, Bough R, Dayan FE (2017) Allelopathic potential of sorghum (Sorghum bicolor (L.) Moench) in weed control: a comprehensive review. In: Advances in Agronomy, vol 145. Academic Press, pp 43–95
Gobena D, Shimels M, Rich PJ, Ruyter-Spira C, Bouwmeester H, Kanuganti S, Mengiste T, Ejeta G (2017) Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. Proc Natl Acad Sci 114:4471–4476
Gurney AL, Grimanelli D, Kanampiu F, Hoisington D, Scholes JD, Press MC (2003) Novel sources of resistance to Striga hermonthica in Tripsacum dactyloides, a wild relative of maize. New Phytol 160:557–568
Gurney AL, Slate J, Press MC, Scholes JD (2006) A novel form of resistance in rice to the angiosperm parasite Striga hermonthica. New Phytol 169:199–208
Kaewchumnong K, Price AH (2008) A study on the susceptibility of rice cultivars to Striga hermonthica and mapping of Striga tolerance quantitative trait loci in rice. New Phytol 180:206–216
Karaya H, Njoroge K, Mugo SN, Ariga ES, Kanampiu F, Nderitu JH (2012) Determination of levels of Striga germination stimulants for maize gene bank accessions and elite inbred lines. Int J Plant Prod 6:209–224
Li J, Timko MP (2009) Gene-for-gene resistance in Striga-cowpea associations. Science 325:1094
Maiti RK, Ramaiah KV, Bisen SS, Chidley VL (1984) A comparative study of the haustorial development of Striga asiatica (L.) Kuntze on sorghum cultivars. Ann Bot 54:447–457
Mbuvi DA, Masiga CW, Kuria EK, Masanga J, Wamalwa M, Mohamed A, Odeny D, Hamza N, Timko MP, Runo SM (2017) Novel sources of witchweed (Striga) resistance from wild sorghum accessions. Front Plant Sci 8:116
Mohamed AH, Housley TL, Ejeta G (2010) Inheritance of hypersensitive response to Striga parasitism in sorghum [Sorghum bicolor (L.) Moench]. Afr J Agric Res 5:2720–2729
Mutinda SM, Masanga J, Mutuku JM, Runo S, Alakonya A (2018) KSTP 94, an open-pollinated maize variety has postattachment resistance to purple witchweed (Striga hermonthica). Weed Sci 66:525–529
Mutuku JM, Yoshida S, Shimizu T, Ichihashi Y, Wakatake T, Takahashi A, Seo M, Shirasu K (2015) The WRKY45-dependent signaling pathway is required for resistance against Striga hermonthica parasitism. Plant Physiol 168:1152–1163
Nickrent DL (2018) Number of genera and species of parasitic plants (updated 9/25/18). http://www.parasiticplants.siu.edu/ParPlantNumbers.pdf
Oswald A, Ransom JK (2004) Response of maize varieties to Striga infestation. Crop Prot 23:89–94
Parra-Londono S, Kavka M, Samans B, Snowdon R, Wieckhorst S, Uptmoor R (2018) Sorghum root-system classification in contrasting P environments reveals three main rooting types and root-architecture-related marker–trait associations. Ann Bot 121:267–280
Pérez-Vich B, Velasco L, Rich PJ, Ejeta G (2013) Marker-assisted and physiology-based breeding for resistance to root parasitic Orobanchaceae. In: Joel DM et al (eds) Parasitic orobanchaceae. Springer, Berlin, pp 369–391
Rich PJ (2018) Blowing the dog whistle. New Phytol 218:404–406
Rich PJ (2020) Genetic and management options for controlling Striga. In: Tonapi VA et al (eds) Sorghum in the 21st Century: food–fodder–feed–fuel for a rapidly changing world. Springer, Singapore, pp 421–451
Rich PJ, Ejeta G (2008) Towards effective resistance to Striga in African maize. Plant Signal Behav 3:618–621
Rich PJ, Grenier C, Ejeta G (2004) Striga resistance in the wild relatives of sorghum. Crop Sci 44:2221–2229
Rodenburg J, Cissoko M, Kayongo N, Dieng I, Bisikwa J, Irakiza R, Masoka I, Midega CAO, Scholes JD (2017) Genetic variation and host–parasite specificity of Striga resistance and tolerance in rice: the need for predictive breeding. New Phytol 214:1267–1280
Saluja M, Zhu F, Yu H, Walia H, Sattler SE (2021) Loss of COMT activity reduces lateral root formation and alters the response to water limitation in sorghum brown midrib (bmr) 12 mutant. New Phytol 229:2780–2794
Samejima H, Babiker AG, Mustafa A, Sugimoto Y (2016) Identification of Striga hermonthica-resistant upland rice varieties in Sudan and their resistance phenotypes. Front Plant Sci 7:634–645
Schlemper TR, Leite MF, Lucheta AR, Shimels M, Bouwmeester HJ, van Veen JA, Kuramae EE (2017) Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol Ecol 93:1–8
Swarbrick PJ, Huang K, Liu G, Slate J, Press MC, Scholes JD (2008) Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. New Phytol 179:515–529
Weerasuriya Y, Siame BA, Hess D, Ejeta G, Butler LG (1993) Influence of conditions and genotype on the amount of Striga germination stimulants exuded by roots of several host crops. J Agric Food Chem 41:1492–1496
Yacoubou AM, Zoumarou Wallis N, Menkir A, Zinsou VA, Onzo A, Garcia-Oliveira AL, Meseka S, Wende M, Gedil M, Agre P (2021) Breeding maize (Zea mays) for Striga resistance: past, current and prospects in sub-Saharan Africa. Plant Breeding 140:195–210
Yoda A, Mori N, Akiyama K, Kikuchi M, Xie X, Miura K, Yoneyama K, Sato-Izawa K, Yamaguchi S, Yoneyama K, Nelson DC (2021) Strigolactone biosynthesis catalyzed by cytochrome P450 and sulfotransferase in sorghum. New Phytol 232:1999–2010
Zenna N, Senthilkumar K, Sie M (2017) Rice production in Africa. In: Chauhan BS et al. (eds) Rice production worldwide. Springer, Cham, pp 117–135
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
The opinions expressed in this chapter are those of the author(s) and do not necessarily reflect the views of the IAEA: International Atomic Energy Agency, its Board of Directors, or the countries they represent
Open Access This chapter is licensed under the terms of the Creative Commons Attribution 3.0 IGO license (http://creativecommons.org/licenses/by/3.0/igo/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the IAEA: International Atomic Energy Agency, provide a link to the Creative Commons license and indicate if changes were made.
Any dispute related to the use of the works of the IAEA: International Atomic Energy Agency that cannot be settled amicably shall be submitted to arbitration pursuant to the UNCITRAL rules. The use of the IAEA: International Atomic Energy Agency's name for any purpose other than for attribution, and the use of the IAEA: International Atomic Energy Agency's logo, shall be subject to a separate written license agreement between the IAEA: International Atomic Energy Agency and the user and is not authorized as part of this CC-IGO license. Note that the link provided above includes additional terms and conditions of the license.
The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
Copyright information
© 2024 IAEA: International Atomic Energy Agency
About this chapter
Cite this chapter
Rich, P.J. (2024). Striga as a Constraint to Cereal Production in Sub-Saharan Africa and the Role of Host Plant Resistance. In: Ghanim, A.M.A., Sivasankar, S., Rich, P.J. (eds) Mutation Breeding and Efficiency Enhancing Technologies for Resistance to Striga in Cereals. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-68181-7_1
Download citation
DOI: https://doi.org/10.1007/978-3-662-68181-7_1
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-662-68180-0
Online ISBN: 978-3-662-68181-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)