Mini-review Received: 9 July 2008
Revised: 6 October 2008
Accepted: 16 October 2008
Published online in Wiley Interscience: 16 February 2009
(www.interscience.wiley.com) DOI 10.1002/ps.1726
Strigolactones: structures and biological activities Koichi Yoneyama,∗ Xiaonan Xie, Kaori Yoneyama and Yasutomo Takeuchi Abstract Strigolactones released from plant roots induce seed germination of root parasitic weeds, witchweeds (Striga spp.) and broomrapes (Orobanche spp.), and hyphal branching of symbiotic arbuscular mycorrhizal (AM) fungi. In addition to these functions in the rhizosphere, strigolactones have recently been shown to be a novel class of plant hormones regulating shoot outgrowth. The natural strigolactones identified so far have the common C–D ring moiety, which is thought to be the essential structure for exhibiting biological activity. The introduction of substitutions on the A–B ring moiety of 5-deoxystrigol, the basic strigolactone, affords various strigolactones, e.g. hydroxylation on C-4, C-5 and C-9 leads to orobanchol, strigol and sorgomol respectively. Then, acetylation and probably other derivatisations of these hydroxy-strigolactones would occur. Although the C-2 -(R) stereochemistry was thought to be an important structural feature for potent germination stimulation activity, 2 -epi-strigolactones were found in root exudates of tobacco, rice, pea and other plant species, indicating that at least some plants produce both epimers. c 2009 Society of Chemical Industry Keywords: strigolactone; germination stimulant; parasitic weeds; arbuscular mycorrhizal fungi
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INTRODUCTION
Since the isolation of strigol as a germination stimulant for Striga lutea Lour. from root exudates of a false host cotton (Gossypium hirsutum L.),1,2 more than ten strigol-related compounds, collectively called strigolactones, have been identified as germination stimulants for root parasitic weeds, witchweeds (Striga spp.), broomrapes (Orobanche spp.) and Alectra. Recently, strigolactones were also found as host recognition signals for arbuscular mycorrhizal (AM) fungi, from which plants benefit.3 Since >80% of land plants form symbiotic relationships with AM fungi, these mycotrophics are expected to produce and release strigolactones.4 Surprisingly, not only host plants but also non-hosts of AM fungi such as Arabidopsis sp.5 and white lupin6 produce strigolactones. Such a wide distribution of strigolactones in the plant kingdom indicates that strigolactones have other important roles in plants and in rhizosphere communication. Recent findings unveiled such a hidden function of strigolactones as a novel class of plant hormones regulating shoot branching.7,8 This paper will focus on the structures and biological activities of strigolactones. More detailed discussions on the chemistry and regulation of production of strigolactones can be found in other papers in this issue.9,10
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STRUCTURES OF STRIGOLACTONES
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∗
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Correspondence to: Koichi Yoneyama, Weed Science Centre, Utsunomiya University, 350 Mine-machi, Utsunomiya 321-8505, Japan. E-mail:
[email protected] Weed Science Centre, Utsunomiya University, 350 Mine-machi, Utsunomiya 321-8505, Japan
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2.1 Essential structural features and structural diversity Natural strigolactones isolated to date are shown in Fig. 1. Strigol (1) and strigyl acetate (2) were isolated from cotton root exudates as the first strigolactones.1,2 Strigol was then identified in the root exudates of Striga hosts, sorghum [Sorghum bicolor ¨ (L.) Monch], maize (Zea mays L.) and proso millet (Pennisetum glaucum R.Br.).11 Sorgolactone (3) and alectrol were isolated from root exudates of sorghum12 and cowpea (Vigna unguiculata
Auct.)13 respectively. Isolation of orobanchol (4) and alectrol as the first Orobanche germination stimulants from red clover (Trifolium pretense L.) root exudates clearly demonstrated that both Striga and Orobanche utilise strigolactones as germination cues.14 Recently, alectrol was identified as orobanchyl acetate (5).15,16 5-Deoxystrigol (6), the first identified branching factor for AM fungi from Lotus japonicus (Regel) Larsen root exudates,3 has been detected in root exudates of various plant species, both monocots17 and dicots,6 suggesting that the other strigolactones are derived from 5-deoxystrigol (6).18 – 20 Indeed, an allylic hydroxylation of 5-deoxystrigol (6) leads to strigol (1) or orobanchol (4), and the third hydroxy-strigolactone, sorgomol (7),21 is produced by hydroxylation on the homoallylic position. These hydroxy-strigolactones may be acetylated, and conjugations with sugars and amino acids may occur. Further oxidation of the hydroxymethyl group of sorgomol (7) and subsequent decarboxylation affords sorgolactone (3).20,21 Among the three hydroxy-strigolactones, orobanchol (4) seems to be distributed most widely in the plant kingdom, and various strigolactones that would be derived from orobanchol (4) have been isolated. For example, very recently, 7-oxoorobanchol (8), 7-oxoorobanchyl acetate (9) and 7-hydroxyorobanchol acetate (10) have been detected in flax (Linum usitatissimum L.) and cucumber (Cucumis sativus L.) root exudates.22 The didehydroorobanchol isomers and solanacol (11) detected in the root exudates of tobacco (Nicotiana tabacum L.)23 and tomato
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Figure 1. Chemical structures of natural strigolactones and synthetic analogue GR24; strigol (1), strigyl acetate (2), sorogolactone (3), orobanchol (4), orobanchyl acetate (5), 5-deoxystrigol (6), sorgomol (7), 7-oxoorobanchol (8), 7-oxoorobanchyl acetate (9), 7-hydroxyorobanchyl acetate (10), solanacol (11), 2 -epiorobanchol (12) and fabacyl acetate (ent-2 -epi-4a,8a-epoxyorobanchyl acetate) (13). Please note that the stereochemistry of C-2 in 10 and 11 and that of C-7 in 10 have not been determined.
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(Solanum lycopersicum L.)24 are probably formed via these oxidised orobanchol derivatives. No strigolactones structurally related to strigol (1), except for strigyl acetate (2), have been isolated so far. Tentative structures of didehydro-orobanchol isomers (14–16) are shown in Fig. 2, in which the structures of two strigolactones 17 and 18 detected in cucumber root exudates are included. Through extensive structure–activity relationship (SAR) studies of strigolactones, the C–D ring moiety appeared to be the essential structure for stimulating germination of root parasitic weed seeds.25 – 27 In fact, all natural strigolactones isolated to date contain this structure, as shown in Fig. 1. Until the identification of 2 -epiorobanchol (12) from root exudates of tobacco (N. tabacum),23 natural strigolactones were thought to have 2 -(R) stereochemistry. In addition to tobacco, rice plants (Oryza sativa L. cv. Nipponbare) appeared to produce and exude 5-deoxystrigol, orobanchol and their 2 -epimers (Yoneyama K, unpublished). Some leguminous plants, including garden pea (Pisum sativum L.), produce fabacyl acetate (ent-2 -epi-4a,8a-epoxy-orobanchyl acetate) (13), in detectable amounts, but not its epimer.28 These results suggest that the coupling of the D ring to the ABC part may not be a stereoselective process, and only one enantiomer might be released to the rhizosphere.
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3 BIOLOGICAL ACTIVITY OF STRIGOLACTONES 3.1 Germination stimulation activity As described earlier, extensive studies on the SAR of strigolactones in germination stimulation of root parasitic weed seeds were conducted after the discovery of strigol (1), and the essential structure, the C–D ring moiety, for exhibiting germination stimulation activity has been identified. Natural strigolactones carrying this moiety have moderate to potent germination activity, and they show different levels of activity on each parasite species. In general, acetates of hydroxy-strigolactones (and probably other conjugated strigolactones) are about 10–100-fold less active than the corresponding free hydroxy-strigolactones.16,29 Orobanchyl acetate (alectrol) (5), however, is highly active in Striga gesnerioides Vatke seed germination, which is not elicited by the synthetic strigolactone GR24.13 In addition, 7-oxoorobanchyl acetate (9) was more active than 7-oxoorobanchol (8) on both Orobanche minor Sm. and O. ramosa L. seed germination.22 Since these acetates are chemically more stable than the corresponding hydroxy-strigolactones, they may remain active long enough to induce hyphal branching of AM fungi and seed germination of root parasites in the soil. Conversely, instability of hydroxystrigolactones would restrict their involvement in chemical communication in the rhizosphere.
c 2009 Society of Chemical Industry
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Strigolactones: structures and biological activities
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Figure 2. Tentative chemical structures of didehydro-orobanchol isomers (14–16) and two novel strigolactones (17, 18) in cucumber root exudates.
Strigolactones released to the rhizosphere are subjected to both abiotic and biotic degradations. In general, strigolactones are more stable in acidic soils, but a rapid loss was observed in alkaline soils.30 – 33 Such a rapid loss would mainly be due to the alkaline hydrolysis of these molecules,30 but microbial degradations would also be involved in the dissipation of strigolactones under field conditions. So far, no studies have been conduced on the metabolism of strigolactones in planta or in soil. The C-2 -(R) stereochemistry has been reported to be another important structural feature, and indeed 2 -epi-strigol34 and 2 epi-sorgolactone35 are far less active than their (R)-epimers. Similar trends were observed for the synthetic analogue GR24, where the ‘natural stereoisomer’ was more active than the 2 -epi isomer.36 However, 2 -epiorobanchol (12) is slightly more active than orobanchol (4) on seed germination of O. minor and O. ramosa.23 The introduction of a 4-α-hydroxyl group appears to increase the activity, in particular, in 2 -epi-strigolactones. For example, solanacol (11), 4-α-hydroxy-5,8-dimethyl-GR24, is far more active than GR24,23 while the introduction of a methyl group at C-6 or C-8 did not affect germination stimulation activity.37 Germination stimulation activity of strigolactones on one root parasitic plant species may be different from that on another species. In addition, they may exhibit different potencies in different germination assay systems. Under laboratory conditions, sorgomol (7), originally isolated from sorghum root exudates and then identified in root exudates from white lupin, etc., is more active on Striga than on Orobanche.21 All the plant species examined so far have been shown to exude mixtures of strigolactones. Individual strigolactones in these mixtures may be different even among cultivars within the same plant species, as in the case of sorghum.17 Furthermore, the amounts and ratios of strigolactones seem to vary with growth stages and growth conditions. Hence, under field conditions, the seeds of root parasites and also hypha and spores of AM fungi in the soil will be exposed to constantly changing mixtures of strigolactones. Therefore, synergistic and/or antagonistic interactions among different strigolactones should be examined to understand the host specificity of these organisms.
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3.3 Shoot branching inhibition Very recently, strigolactones, or their metabolites, were reported to be a novel class of plant hormones inhibiting shoot branching.7,8 So far, only the synthetic strigolactone GR24 has been shown to be active in bioassays for shoot branching inhibition, and bioactive form(s) of this new hormone have not been clarified. In pea ccd8 and rice d10 mutants, levels of orobanchyl acetate (5) and fabacyl acetate (13)7 and the level of 2 -epi-5-deoxystrigol (14),8 respectively, were significantly reduced, and therefore it is likely that other natural and synthetic strigolactones that induce parasite seed germination also inhibit shoot branching. To clarify bioactive form(s) of this hormone, rapid and sensitive bioassays need to be developed.
4
CONCLUSION
It is likely that plants produce mixtures of strigolactones and release them into the rhizosphere. Therefore, seeds of root parasites are exposed to strigolactones if they are located close to a living root of any plant species. This is also true for AM fungi. However, both seed germination of parasites and hyphal branching of AM fungi are often reduced in the vicinity of non-host roots. Therefore, not only strigolactones but also other signalling chemicals that are synergistic or antagonistic to strigolactone action are involved in the seed germination of root parasitic weeds and hyphal branching of AM fungi. Further study is needed to clarify why plants produce so many different strigolactones and how each strigolactone contributes to host recognition by root parasites and by AM fungi. To establish an affordable management strategy of root parasitic weeds, it must be taken into consideration that strigolactones are host recognition signals for both symbiosis and parasitism.
ACKNOWLEDGEMENTS Part of the study was supported by a Grant-in-Aid for Scientific Research (1820810) from the Japanese Society for the Promotion of Science (JSPS).
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3.2 Hyphal branching activity The natural strigolactones identified so far have been examined for their activity on hyphal branching in AM fungus Gigaspora margarita Becker & Hall. In general, structural requirements for activity are very similar to those for germination stimulation
of root parasites, and all natural strigolactones are active as branching factors (Akiyama K, unpublished). Details will be published elsewhere.
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