Secondary metabolite signalling in host–parasitic plant interactions

https://doi.org/10.1016/S1369-5266(03)00065-7Get rights and content

Abstract

The parasitic weeds Orobanche and Striga spp. are a serious threat to agriculture in large parts of the world. The lifecycle of the parasitic weeds is closely regulated by the presence of their hosts, and secondary metabolites that are produced by host plants play an important role in this interaction. Model plants, such as Arabidopsis and maize mutant collections, have been increasingly used to study these chemical signals, especially those host-produced stimulants that induce the germination of parasite seeds.

Introduction

In large parts of the world, parasitic weeds are among the most damaging agricultural pests. Of the 28 Striga spp., S. asiatica, S. aspera, S. forbesii and particularly S. hermonthica (Figure 1d) parasitise cereal crops such as sorghum, maize, millet and rice. These parasite species infest about two-thirds of the 70 million hectares used for cereal production in Africa and negatively affect the lives of some 300 million people 1., 2., 3.. Striga gesnerioides is also a pervasive parasitic weed that infects dicotyledonous crops such as cowpea [4]. Of the more than 100 Orobanche spp., only O. crenata, O. ramosa, O. cumana and O. aegyptiaca parasitise agricultural crops. They affect crops such as legumes, crucifers, tomato, sunflower, hemp and tobacco in the Middle East, India and large parts of Europe and North America 3., 5.. The tremendous impact of parasitic plants on world agriculture has prompted much research aimed at preventing infestation. A variety of approaches have been taken, including seeking better agronomic practices and breeding for resistance [3]. In this review, however, we focus on the importance of chemical signalling in the interaction between host and parasite.

Section snippets

Signalling between host and parasite

Although Striga and Orobanche species parasitise different hosts in different parts of the world, their lifecycles are broadly similar. Hence, we will discuss the two genera together. The important steps in the lifecycle are germination, radicle growth to the host root, haustorium formation and attachment to the host root, establishment of a xylem connection and a compatible interaction, and seed production (Figure 1). Extensive signalling between the host plant and the parasite features in

Germination stimulants

Three classes of compounds have been described that have germination-stimulating activity: dihydrosorgoleone, the strigolactones and the sesquiterpene lactones (Figure 2). In particular, the nature of germination factors from sorghum has been debated [13]. Lynn and coworkers [9] suggest that dihydrosorgoleone is the active stimulant in the root exudates of sorghum and other monocotyledonous hosts. It has been suggested, however, that dihydrosorgoleone is less likely to be the germination

Host specificity and parasite control

The chemical structures of the four strigolactones identified to date are small variations on one molecular backbone (Figure 2). It is tempting to speculate that these small variations play a role in the host specificity of the parasitic weeds. Recognition of particular germination stimulants may ensure that the seeds of parasites only germinate in the presence of a true host. However, several examples show that the germination responses of parasitic seeds may not be very specific. Wigchert and

Biosynthetic origin of germination stimulants

Surprisingly, little is known about the biosynthesis pathway for germination stimulants in the roots of the host species or about how this pathway is regulated. This lack of knowledge is due to the extremely low concentrations of highly active compounds that are produced by and secreted from the host roots. The strigolactones have been described as sesquiterpene lactones by many authors. However, the structures bear similarities to higher terpenoids and may be derived from them (MH Beale, HJ

Conclusions

Host-derived secondary metabolites play an important role in the interaction between parasitic weeds and their hosts. They are involved in signalling, for example in the induction of parasite germination and the formation of the haustorium, and in plant defence against the parasite (e.g. phytoalexins). Although it is unlikely that the germination stimulants alone determine host specificity, they are responsible for the first step in the lifecycle of parasitic weeds and hence are an important

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

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    of outstanding interest

Acknowledgements

We thank J Beekwilder and R de Maagd for helpful comments on the manuscript. We acknowledge funding from the European Commission (INCO-DEV, ICA4-CT-2000-30012 [to HJB and MHB]); the Dutch Ministry of Agriculture, Nature Management and Fisheries in the form of an IAC-fellowship (to RM) and funding from the North-South programme (to HB); the Netherlands Foundation for the Advancement of Tropical Research (WOTRO [to SZ]); the Netherlands Organisation for Scientific Research (NWO [NATO-visiting

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