Review
Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants

https://doi.org/10.1016/j.plaphy.2008.04.012Get rights and content

Abstract

Parasitic plants cause devastating losses to crop yields in several parts of the world. The root parasites, Striga and Orobanche species, use chemical signalling molecules that are exuded by the roots of plants in extremely low concentrations, and that can induce germination of the seeds of these parasites, to detect the vicinity of a suitable host. The majority of the so far identified germination stimulants belong to the strigolactones. It was recently discovered that this class of compounds can also induce hyphal branching in the symbiotic arbuscular mycorrhizal fungi, a process involved in root colonisation. The elucidation of the structure of new strigolactones is hindered by their low abundance and instability. In the present paper, we have used existing knowledge on the structure of strigolactones and combined it with recently obtained insight in the biosynthetic origin of these signalling compounds. This enabled us to postulate structures for strigolactones that have been isolated but for which so far the structure has not been elucidated, but also to propose structures of strigolactones that may be discovered in the future. Considering the strongly increased importance of the strigolactones, we expect that more groups will look for these compounds and also in systems so far not exploited. This could lead to the discovery of new strigolactones for which we expect the present biogenetic considerations will facilitate identification and structure elucidation.

Introduction

Parasitic plants of the Striga, Alectra and Orobanche genera (Orobanchaceae) are noxious root parasites on many food crops and cause devastating losses to crop yields in several parts of the world. The damage due to these parasitic weeds sometimes reaches up to 100% which results in little or no food at all for millions of people in Africa, India and the Middle East [7], [12], [36], [41]. Control of these parasitic weeds is exceptionally difficult as they produce huge numbers of seeds that remain viable in the soil for many years [5], [12]. Although several control measures, including crop rotation, trap and catch cropping, fallowing, handpulling, inter- and mixed-cropping, synthetic seed germination stimulants (to induce suicidal germination) and the use of resistant varieties, have been explored, the ultimate solution to this problem is still far away [26], [36]. In order to be able to design new and effective control methods for parasitic weeds, detailed insight into their life cycle is of utmost importance. The first step in this life cycle is the germination of seeds of these parasitic plants, which is induced by chemical substances – germination stimulants – exuded from roots of host or non-host (trap) crops [7], [39], [45], [53]. Most of the so far isolated and identified germination stimulants possess the same basic skeleton (Fig. 1) and are collectively called ‘strigolactones’, as was first proposed by Butler [12].

Until recently, the biological function of these strigolactones for the host plant was unknown. However, it was shown that strigolactones are the host-root produced chemical signals that induce hyphal branching in germinating spores of arbuscular mycorrhizal fungi (AM fungi), a process that is probably essential for host-root colonisation by AM fungi [1], [2], [8], [11], [18]. In addition to ‘germination stimulant’ the strigolactones can therefore be called ‘branching factor’. Most of the terrestrial plants have a symbiotic association with AM fungi [35]. The fungi get carbohydrates from the higher plants and supply them with nutrients from the soil. They have also been reported to protect the host plants against draught and pathogen attack [37]. It is considered that plants have evolved to produce strigolactones in order to enable AM fungi to colonise their roots and that parasitic plants are taking advantage of these host-presence signalling molecules to help them sense the vicinity of a host as well [8].

Even before the signalling role of the strigolactones for AM fungi was known, there was a substantial interest in the isolation and identification of these signalling molecules from a range of plant species. The strigolactones are produced by plants in extremely low quantities and may be unstable during the purification process. Therefore, their isolation, purification and structure elucidation are very difficult. So far nine strigolactones – strigol (1), strigyl acetate (2), 5-deoxystrigol (3), orobanchol (4), orobanchyl acetate (5), sorgolactone (6), 2′-epi-orobanchol (7), solanacol (8) and sorgomol (9) (Fig. 1) – have been identified and structurally characterised in the root exudates of various host and non-host plant species [4], [13], [20], [34], [40], [42], [47], [48], [49], [51], [52]. Akiyama et al. [1] demonstrated that 5-deoxystrigol (3) in Lotus japonicus root exudate is the factor that induces hyphal branching in Gigaspora margarita. These authors and others showed that most of the known strigolactones – strigol, sorgolactone and the synthetic germination stimulant GR 24 – do the same [1], [6].

In addition, several novel strigolactones of which the structure has not been elucidated have been reported – such as the two to three didehydro-strigol/orobanchol isomers – in the root exudates of tomato and sorghum [4], [27], [47], [53]. In addition, in the exudates of several other plant species additional unknown strigolactones were detected – such as another putative strigol isomer and putative epi-strigolactones – by us (Goldwasser et al., unpublished results; Charnikhova et al., unpublished results).

The structures assigned for strigolactones (19) (Fig. 1) have been established by physical and spectral data and/or their synthesis [1], [10], [14], [21], [28], [30], [33], [43], [44], [47], [48], [49]. Structures (1012) (Fig. 1) have been proposed for alectrol [34], [46], but it was recently shown that alectrol is orobanchyl acetate [49]. Nevertheless, the proposed structures may be candidate structures for the multitude of uncharacterised strigolactones listed above and/or for strigolactones still to be discovered.

Spectral analysis tools are very powerful in assigning structures to unknown compounds. However, in the case of strigolactones spectral analysis is limited by the very low concentrations in plant exudates and hence their isolation in sufficient amount is difficult. In such cases, knowledge about the biosynthetic origin of these compounds in plants could help in assigning possible structures to unidentified strigolactones. Until recently, however, the biosynthetic origin of the strigolactones was unknown, although they were characterised as sesquiterpene lactones [7]. In studies using inhibitors and mutants of maize (Zea mays) and tomato (Solanum lycopersicum), we demonstrated that the strigolactone germination stimulants of maize, sorghum, cowpea and tomato are not sesquiterpenes but are apocarotenoids [27], [31]. Following that discovery, a biogenetic scheme for the formation of all known strigolactones from a carotenoid precursor was proposed (Fig. 2) [31] (also see [23], [24]). With the subsequent structural identification of strigyl acetate (2), orobanchyl acetate (5), 2′-epi-orobanchol (7), solanacol (8) and sorgomol (9) (Fig. 1) the original scheme can be extended with acetyl ester formation [(2) and (5)], oxidation and methyl transfer (8) and a different stereochemistry for D-ring coupling (7), whereas the structure of sorgomol (9) suggests that hydroxylation on the homoallyl positions of 5-deoxystrigol (3) occurs, followed by further oxidation and decarboxylation of sorgomol to afford sorgolactone (6) (Fig. 2).

In the present communication we elaborate on this biogenetic route in more detail. In addition, the structures for other, so far not identified or characterised, strigolactones are being suggested on the basis of this biogenetic scheme. Although in our schemes we have omitted stereochemistry where it is unknown, stereochemistry must be considered in biological and structure elucidation studies as it may make the difference between an active and an inactive strigolactone [28], [38], [44], [54].

Section snippets

Biogenetic considerations for the structure of unidentified strigolactones

All the strigolactones possess the same basic chemical structure (Fig. 1). The left part of these stimulants comprising rings A, B and C consists of 14 carbons [13 in sorgolactone (6)]. Structurally and biochemically, the most likely candidate substrate among the carotenoids so far reported in higher plants, is 9(Z)-β-carotene which on oxidative cleavage at the Δ11,12 olefinic bond yields a C15 aldehyde (13) that by oxidation and epoxidation followed by the loss of one carbon through

Conclusion

We have used existing knowledge on the structure of strigolactones and combined that with insight in the biosynthetic origin of these important signalling compounds. This enabled us to postulate structures for strigolactones that have been detected but for which so far the structure has not been elucidated, such as the unknown strigolactones detected in several root exudates ([4], [27], [47], [53] and Goldwasser et al., unpublished results; Charnikhova et al., unpublished results) but also to

Acknowledgements

This work was supported by the Netherlands Organisation for Scientific Research (NWO; VICI-grant to HJB), the European Commission (the FP5 EU project Improved Striga Control in Maize and Sorghum; INCO-DEV, ICA4-CT-2000-30012 and the FP6 EU Integrated Project Grain Legumes; FOOD-CT-2004-506223) (to HJB), the Dutch Ministry of Agriculture, Nature Management and Fisheries' North-South programme (to HJB), and the Netherlands Organisation for Scientific Research (NWO; NATO-visiting scientist

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