Strigolactones: new plant hormones in action
The key step in the mode of action of strigolactones is the enzymatic detachment of the D-ring. The thus formed hydroxy butenolide induces conformational changes of the receptor pocket which trigger a cascade of reactions in the signal transduction.
Strigolactones (SLs) constitute a new class of plant hormones which are of increasing importance in plant science. For the last 60 years, they have been known as germination stimulants for parasitic plants. Recently, several new bio-properties of SLs have been discovered such as the branching factor for arbuscular mycorrhizal fungi, regulation of plant architecture (inhibition of bud outgrowth and of shoot branching) and the response to abiotic factors, etc. To broaden horizons and encourage new ideas for identifying and synthesising new and structurally simple SLs, this review is focused on molecular aspects of this new class of plant hormones. Special attention has been given to structural features, the mode of action of these phytohormones in various biological actions, the design of SL analogs and their applications.
KeywordsKarrikins Mode of action Signal transduction Strigolactones Strigolactone analogs Strigolactone mimics
- AM fungi
Arbuscular mycorrhizal fungi
Strigolactones (SLs) constitute a new class of plant hormones which are of increasing importance in plant science. They belong to the group of biologically active molecules called semiochemicals that are used to disseminate information between individual species. Important examples of plants that have become completely dependent on allelochemicals are the parasitic weeds witchweed (Striga spp., Orobanchaceae/Scrophulariaceae) and broomrape (Orobanche spp., Orobanchaceae). The seeds of these weeds only germinate in response to specific chemicals, namely germination stimulants, present in the rhizosphere of host plants and some non-host plants. For these parasitic flowering plants, which are totally dependent on specific association with a host that provides nutrients and water, this system ensures that germination only starts when suitable host roots are available in the immediate vicinity. Other allelochemicals are required to effect attachment of the germinated seeds to the roots of the host plants via a specialised organ, the haustorium. Once the vascular connections between host and parasite have been established, the parasite can develop at the expense of the host plant. As a consequence of providing nutrients to the parasite, the crop yield of the host plant will be severely affected. In many cases of important food crops, this parasitic interaction causes a serious problem in food production.
In recent years several new bio-properties of SLs have been discovered. A real breakthrough was the discovery that SLs act as the branching factor for arbuscular mycorrhizal (AM) fungi (Akiyama et al. 2005; Parniske 2008). Mycorrhizae are symbiotic associations between soil, fungi and plant roots (Akiyama and Hayashi 2006). This interaction is probably the most widespread and significant symbiosis in nature (Brachmann and Parniske 2006). AM fungi are obligate symbionts unable to complete their life cycle in the absence of a suitable host. A critical step in the development of AM fungi is the triggering of the hyphal morphogenesis by a branching factor. The isolation and characterization of a branching factor was extremely difficult due to the fact that their concentrations were very low. The first branching factor was isolated from the roots of hydroponically grown Lotus japonica and it was shown to be (+)-5-deoxystrigol. It was also demonstrated that other SLs, such as strigol and orobanchol, are highly active branching factors. Knowing the identity of the branching factors of AM fungi opens new windows for their practical applications (Akiyama and Hayashi 2006).
A second important breakthrough in SL research followed a few years later. It was then demonstrated that endogenous SLs play an important role in the control of plant architecture. Inhibition of bud outgrowth and inhibition of shoot branching are typical examples (Gomez-Roldan et al. 2008; Umehara et al. 2008). The inhibitory processes are regulated by endogenous cues of which SLs are probably most prominent. Importantly, inhibition of shoot branching could also be induced exogenously by treatment with the synthetic SL GR24. For a long time, involvement of two other classes of plant hormones, namely auxin and cytokinines, has been known in controlling shoot branching. Now, SLs are recognised as a third class of new plant hormones. This control of plant architecture with SLs gave rise to an avalanche of publications on this topic, indicating the high importance of this new role of SLs. Several excellent reviews have appeared on this subject (Tsuchiya and McCourt 2009; Koltai 2011, 2014, 2015; Cheng et al. 2013; Waldie et al. 2014).
In this review, the focus will primarily be on molecular aspects of this intriguing class of new plant hormones. The synthesis of SLs, of both naturally occurring SLs and of synthetic analogs, are reviewed separately (Zwanenburg et al. 2015).
Isolation of SLs
The first SL ever isolated was obtained from root exudates of cotton (Gossypium hirsutum L.) as early as 1966 and was named strigol (Cook et al. 1966). The gross structure of strigol was elucidated in 1972 (Cook et al. 1972) and the full details were determined by means of an X-ray diffraction analysis in 1985 (Brooks et al. 1985) about 20 years after its isolation. Strigol was isolated from a non-host for the parasitic weed Striga and consequently, its significance for the host–parasite interaction was uncertain for a long time. It was not until 1992 that sorgolactone, a compound with a structure similar to strigol, was isolated (Hauck et al. 1992) from root exudates of a true host for Striga, sorghum (Sorghum bicolor L. Moench).
Soon thereafter, alectrol was obtained from the root exudate of cowpea (Vigna unguiculata L.) which is a host for S. gesnerioides (Muller et al. 1992). The collective name ‘strigolactones’ was proposed by Butler, a pioneer in this area (Butler 1995). The isolation of SLs from root exudates is very laborious and requires a careful chromatographic separation accompanied by bioassays for germination of appropriate seeds of parasitic weeds. The production of SLs per plant is very small: 15 pg/day/plant (Sato et al. 2005), hence collection of root exudate from hydroponically grown host plants requires an experimental set-up with many plants. At present the HPLC separation techniques are much more sophisticated and fewer plants are needed. The structural analysis of SLs is a highly demanding exercise using high resolution mass spectrometry and NMR analysis. Especially, establishing the correct stereochemistry needs utmost care.
Naturally occurring SLs
At present two families of naturally occurring SLs are known (Fig. 1). Because of the tricky aspects of the structural analyses, some misassignments were made. For example, establishing the structure of alectrol (Muller et al. 1992) was particularly difficult and it took about two decades before the correct structure was elucidated (Ueno et al. 2011, 2015). The structure of orobanchol, which is probably one of the most abundant SLs, was initially incorrectly assigned (Ueno et al. 2011). Originally it was a logical assumption that the stereochemistry would be as in (+)-strigol (Mori et al. 1999). A third example is solanacol. In the first proposed structure the methyl substituents in the A-ring were positioned para (Xie et al. 2007) instead of ortho (Takikawa et al. 2009), and as far as the stereochemistry is concerned: it belongs to the orobanchol family and not to the strigol family as suggested originally (Chen et al. 2010, 2013). More details about the structural corrections have been reviewed earlier (Zwanenburg and Pospisil 2013).
The occurrence of SLs in nature and the source from where they have been obtained has recently been reviewed and where possible correct structures are included in the tables (Cavar et al. 2015). Moreover, strigolactones play a major role in host specificity of Orobanche and Phelipanche (the broomrapes) seed germination. In general, weedy broomrape species are less specialised in germination requirements than the non-weedy species (Fernandez-Aparicio et al. 2011).
Relevance of stereochemistry in SLs
Establishing the stereochemistry at the respective stereogenic centers was, and still is, a major obstacle in elucidating the correct detailed structure of naturally occurring SLs. For assigning the stereochemistry at C-2′ of the D-ring the empirical rule reported by Welzel et al. (1999), based on the Cotton effect in ORD/CD spectra, is appropriate. For the ABC part, correlation diagrams with compounds of known stereochemistry are mostly used (Zwanenburg and Pospisil 2013). An X-ray diffraction analysis is the most reliable manner to establish the absolute stereochemistry of an SL. However, for that a crystalline sample of the SL is needed which is not always easy to obtain. The stereochemistry has a pronounced effect on the germinating activity towards the seed of parasitic weeds. In addition, for the other SL bio-properties there is a profound effect of the stereochemistry on the bio-response.
Naming protocol for SLs
The SLs have several chiral centers, for example strigol has three such centers and there are 23 = 8 conceivable stereoisomers. From a chemical point of view a correct and unambiguous manner to designate the chirality at the respective stereogenic centers, the use of the Cahn-Ingold-Prelog (CIP) descriptors R and S to indicate the sense of chirality is most appropriate. The R,S notation is based on abstract rules which are not easy to handle. Using the ent and epi prefixes is much easier in practise, whereby ent refers to enantiomer, i.e. mirror image of an entire unit and epi refers to epimer, i.e. opposite configuration at a given atom. For the ent/epi method it is necessary to choose a reference compound, a parent molecule. In the time before the structural correction of orobanchol, the naming of SLs was simple and straightforward: (+)-strigol was the logical parent compound and the stereochemistry of all other SLs was related to that parent compound. However, after the structure change of orobanchol in 2011 (Ueno et al. 2011) there were two options, either to keep the naming protocol with (+)- strigol as the parent or to use the new structure for natural orobanchol as parent compound for the orobanchol family. Both methods are in use, which may lead to confusing situations (Zwanenburg and Pospisil 2013). The reader is forewarned.
Scaffidi et al. (2014) suggested an alternative naming and notation in the structural correlation of GR24 stereoisomers using both (+)-strigol and (−)-orobanchol as standards. This resulted in two names for some stereoisomers, e.g. ent-2′-epi-5-deoxystrigol is also named 4-deoxyorobanchol. This method has little added value and is confusing for those who are less familiar with stereochemical issues.
Simplified SLs with retention of germinating activity: design of SL analogs
It is important to note that these analogs not only must have a simplified structure with retention of germinating activity, but also they must be synthetically readily accessible. An illustrative example of the successful implementation of the model is Nijmegen-1. It can indeed readily be obtained from simple starting materials in a few synthetic steps and its germinating activity is comparable to that of GR24.
GR24 is commonly used as standard in germination studies. Mostly, this stimulant is a racemate in which the relative stereo configuration is as in (+)-strigol. However, it should be noted that not all seeds of parasitic weeds do respond to GR24, for example O. crenata, O. foetida, O. hederae and O. densiflora (Fernandez-Aparicio et al. 2011), as well as O. picridis and O. minor subsp. maritima (Thorogood et al. 2009) do not respond.
SLs as branching factors for AM fungi
Stimulation of AM fungi fulfils a symbiotic role with parasitic plants. After the first observation, much attention was given to the beneficial mutualistic and symbiotic associations of AM fungi and parasitic plants (Akiyama and Hayashi 2006; Bonfante and Requena 2011). AM fungi facilitate the uptake of phosphates and nitrates, and in a sense these fungi serve as soil fertiliser which may be of agricultural value. Knowledge of this symbiotic relationship could provide a new strategy for the management and control of beneficial fungal symbionts and of devastating parasitic weeds in agriculture and natural ecosystems.
SLs as inhibitors for shoot branching and in their role in controlling plant architecture
As mentioned in the introduction, SLs are now recognised as new plant hormones. An important newly discovered activity deals with the control of plant architecture. SLs will not operate standing alone, but in concert with other plant hormones. Until 25 years ago there were 5 types of plant hormones known, namely: auxins, cytokinins, ethene (ethylene), gibberellins and abscisic acid (ABA). More recently, brassinosteroids and jasmonates have been added to the list. The role of the various plant hormones in the plant kingdom is under extensive investigation. There is accumulating evidence that SLs interplay in a crosstalk with several of these plant hormones. Which endogenously SLs are operative in the interplay in planta is unknown in most cases. The crosstalk of SLs with other plant hormones may either take place in a fully concerted manner or sequentially in a cascade of events, although in many cases the precise modus operandi is not known in detail. Phenomenologically, the crosstalk interactions are well documented.
As it is common for other phytohormones, the SL biosynthesis and activity is regulated by other hormones. For instance, cytokinins act as antagonists to SLs in regulation of axillary bud outgrowth (Dun et al. 2012) and in regulation of mesocotyl elongation in darkness (Hu et al. 2014). Auxins are not only shown as one of the major regulators of SL biosynthesis (Hayward et al. 2009; Al-Babili and Bouwmeester 2015, and references therein), but also they act as antagonists because SLs may enhance auxin transport (Cheng et al. 2013, and references therein). Lopez-Raez et al. (2010) showed that abscisic acid, one of the key regulators of plant response to abiotic stress, has a role in SL biosynthesis, but, on the other hand SLs can also impact biosynthesis of abscisic acid (Al-Babili and Bouwmeester 2015). Besides phytohormones, it is well established that phosphate affects SL biosynthesis, meaning that shortage of phosphate increases SL production (Koltai 2015, and references therein).
However, all these facts are still on cellular level, and they do not explain on a molecular basis which exact mechanisms play a role. This is a highly complex research area due to the different effects of phytohormones and varying context of their actions.
Most studies on the control of plant architecture are carried out with increased branching mutants, predominantly with ramosus (rms) in garden pea (Pisum sativum), more axillary growth (max) in Arabidopsis (Arabidopsis thaliana), decreased apical dominance (dad) in Petunia hybrida and dwarf (d) and high tillering dwarf (htd) in rice (Oryza sativa). Treatment with an exogenous SL, practically in all cases synthetic GR24 was employed, resulted in the inhibition of shoot branching (Dun et al. 2013), stimulation of internode growth (de Saint et al. 2013), acceleration of leaf senescence (Yamada et al. 2014), enhance root hair elongation and the growth of primary roots (Kapulnik et al. 2011), inhibition of the outgrowth of axillary buds (Minakuchi et al. 2010), inhibition of formation of adventitious and lateral roots (Rasmussen et al. 2012a, b, 2013a, b), increasing stem thickness and inducing secondary growth (Agusti et al. 2011) and other morphological changes. It was found that auxin–SL interactions at multiple levels are critical for branching control (Stirnberg et al. 2010; Koltai et al. 2010). How these inhibitory processes work on a molecular level is still unknown. The plant physiology and biology of the control plant architecture induced by SLs are beyond the scope of this review. The relevant details of these aspect of the control of plant architecture on the cellular level are summarised in several excellent reviews (Tsuchiya and McCourt 2009; Koltai 2011, 2014, 2015; Cheng et al. 2013; Waldie et al. 2014).
SL mimics (Fig. 9) with an inhibitory effect on shoot branching of rice mutants d10-1 were reported by the Asami group (Fukui et al. 2011, 2013). All these mimics, which are also named as debranones (furanones showing de-branching activity), have O-aryl substituents at C-2′ of the butenolide ring. Mimics with a Br or a CN group in the para position are the most active ones. These compounds resemble the SL mimic reported by Boyer et al. having an S-atom at C-2′. Again, it is not made sure whether the O-aryl group is required for activity. Note that these debranones are also moderately active as germinating agents (see section SL mimics).
SLs and karrikinolides (smoke compounds)
The KAR structure is planar and achiral, contains two annelated rings, whilst SLs have at least one chiral center, one of them at the five-membered D-ring. The five-membered ring in SLs can rotate freely while in KARs it is constraint in a rigid bicyclic system. The KARs contains an exo-methylene group at the γ-carbon of the lactone, while in SLs this is an acetal type group. It is evident, from the molecular point of view, that the compounds are quite different entities, each with its own reactivity pattern with practically no common features. In spite of this, KARs are germination stimulants for seeds of Solanum orbiculatum, but not for seeds of parasitic weeds (Flematti et al. 2010).
It is perfectly alright to discuss KARs in the same context as SLs because they both are germination stimulants, albeit for different seed types. However, the justification that is frequently encountered in the literature, namely that both stimulants contain a similar butenolide unit is simply not correct.
Mode of action of SLs
More recently, several studies of protein structures were reported which shed new light on the signal perception of SLs especially in SLs in shoot and branching inhibition (Hamiaux et al. 2012; Guo et al. 2013; Kagiyama et al. 2013; Nakamura et al. 2013; Zhao et al. 2013). The DAD2 gene was identified from petunia which encodes for an α/β hydrolase protein DAD2 (Hamiaux et al. 2012). Similarly, rice genome D14 encodes for the protein D14 (DWARF14) and a closely related homolog D14-LIKE (D14L) (Kagiyama et al. 2013; Zhao et al. 2013). The latter is also referred to as KARRIKIN INSENSITIVE 2 (KAI2) present in Arabidopsis and which is specific to karrikins (KARs) (Arite et al. 2009). The role of the D14 gene products, whose sequence suggests that they belong to the α/β-fold hydrolase super family, received much attention because members of the α/β fold hydrolase superfamily are known to participate in hormone signalling for instance those involving gibberellin (GA) and the receptor GID1 (Ueguchi-Tanaka et al. 2005; Murase et al. 2008). The three protein structures, DAD2, D14 and KAI2 are almost superimposable, implying that they are orthologs.
The crystal structure of the protein DAD2 reveals an α/β hydrolase fold containing a canonical catalytic triad Ser-His-Asp with a large cone-shaped internal cavity capable of accommodating SLs (Hamiaux et al. 2012). The protein was incubated with racemic GR24 in a 1:20 ratio. After 18 h, no GR24 was left and formyl tricyclolactone (ABC=CHOH) resulting from the hydrolysis of GR24 was isolated by chromatography along with an unknown second product (probably an artifact) (Hamiaux et al. 2012). On the basis of this hydrolytic detachment of the D-ring it was proposed that SLs are essential for the signal transduction, in spite of the fact that the conditions for this hydrolysis experiment were far from biomimetic; similarly, incubation of D14 with GR24 resulting in hydrolysis products ABC=CHOH and hydroxy butenolide (D–OH) (Zhao et al. 2013; Nakamura et al. 2013). The latter most detailed study (Nakamura et al. 2013) revealed that the hydrolysis induced by D14 is stereospecific. (+)-GR24 underwent hydrolysis much faster than its antipode (−)-GR24. Differential scanning fluorimetry (DCF) measurements of DAD2 with increasing amounts of GR24 indicated a binding of GR24 with DAD2 in the ratio of 2:1. DCF measurements were also used to establish the interaction of SLs (GR24) with the protein D14 (Kagiyama et al. 2013).
Co-crystallisation of GR24 with D14 could not be accomplished. Zhao et al. (2013) observed in an attempted co-crystallisation experiment of rice D14 and GR24 an electron density that was assigned to 2,4,4-trihydroxy-3-methyl-3-butenal [(HO)2C=C(Me)-CH(OH)-CH=O] which was proposed as an intermediate en route to hydroxy butenolide (HO-D). Its formation was rationalised by an acyl transfer reaction (see Fig. 12, compared Scaffidi et al. 2012, mechanistically not generally accepted behaviour of esters) involving the D-ring and the serine unit of the catalytic triad to give the ring-opened product [SerCH2OC(=O)C(Me)=CHCH=O] which is then suggested to undergo a rotation around the olefinic bond (an energetically highly demanding conversion, unlikely to occur in the crystal lattice at ambient temperature) to give isomeric HO2CC(Me)=CH–CH=O. Subsequent addition of water to the –CH=C(Me)CO2H moiety gives the intermediate bound to Ser. Lactonization and elimination of water then results in HO-D. This sequence of events with two questionable steps lacks underpinning and is not an adequate explanation for the detachment of HO-D without further confirmation.
The interaction of the karrikins (KARs) with KAI2 protein was also clarified using an X-ray structure. Interestingly, it was found that the karrikin molecule is not hydrolyzed by the protein (Janssen and Snowden 2012; Guo et al. 2013). The KAR molecule is situated in the opening to the active site close to a helical domain but distal from the canonical catalytic triad of the α/β/hydrolase. Without undergoing any molecular change KAR is inducing a conformational change in the KAI2 protein which initiates the signal transduction production process in close analogy to the mode of action of gibberellins. It should be noted that this mode of action of KAR demonstrates that SLs and KARs are entirely different molecular entities, as already outlined in Fig. 10.
All these compounds are remarkably active as germinating agents. After hydrolytic detachment of HO-D by interaction with the protein, ABC=CHOH fragment carrying the large substituent will undoubtedly be expelled from the active cavity. As a consequence, a fluorescent signal was measured upon interaction with a seed of a parasitic weed, may be due to the expelled fragment and not to the fluorescent SL in the receptor protein. In addition, protein fishing experiment may be frustrated by the enzymatic detachment of HO-D and the concurrent removal of the labelled ABC fragment from the protein. The ‘hook’ in the protein is detached from the ‘fishing line’ which is expelled.
The first attempts on the identification of a receptor protein of S. hermonthioca were reported recently (Toh et al. 2015). Using expression in Arabidopsis, it was shown that ShHTLs [Striga HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE 2 (HTL/KAI2); diverged family of α/β hydrolase-fold proteins related to D14] might be good candidates. However, isolation of a receptor protein from seeds of parasitic weeds has not yet been achieved.
For the debranone type SLs (Fig. 6), a different mode of action must be operative. This pathway has to account for the observation that 3,4-dimethyl-5-p-chlorophenylthio-butenolide (see Fig. 9) is highly active in shoot branching control (Boyer et al. 2012, 2014). This implies that a Michael addition of water at C-4 of the D-ring cannot be part of the mode of action on the protein level.
Now it may be concluded that the mode of action of SLs, SL analogs and SL mimics show a consistent picture in all cases, the release of HO-D is the essential prime trigger for the cascade of reactions leading to the signal transduction.
Applications of SLs
SLs, their analogs and mimics have a great potential for applications in agriculture. The control of parasitic weeds is under active investigation. One option for this is the suicidal germination approach. A germination stimulant, preferably a readily accessible synthetic analog, is applied to the field in the absence of a host. Seed of the weed will germinate but due to the lack of nutrients they die. After that the host plant, usually an important crop, can be planted which then does not suffer anymore from the parasitizing weed (Zwanenburg et al. 2009). Details will be described in a forthcoming review (Zwanenburg, accepted for publication in Pest Manag Sci).
The recent finding that SLs play an essential role in the control of plant architecture led to extensive studies to improve the structure of agriculturally important plants. Details are, however, beyond the scope of this review.
Conclusions and future outlook
The area of strigolactones is rapidly evolving. In recent years much new insight was obtained in the structure and bio-properties of naturally occurring SLs, but there is still much to gain. Reliable models have been developed for the design and synthesis of SL analogs with excellent bio-activity, but further fine tuning is necessary. The SL mimics constitute an important new group of simple compounds with a high bio-activity. Further development of SL mimics is highly relevant, also in connection with possible applications. Insight into the mode of action has been considerably improved. A consistent picture for SLs, SL analogs and SL mimics has been developed, but more information is needed to fully understand the interaction of SLs, its analogs and mimics with proteins. The role of SLs in planta for the control of plant architecture received much attention and will do so in the years to come. So far the protein receptors of seeds of parasitic weeds and AM fungi have not been isolated and identified; here lies an interesting challenge for the future. The molecular understanding of processes in which SLs play a dominant role is of utmost importance and may provide new leads for future research in this exciting area of plant hormones.
Author contribution statement
BZ (senior author) 60 %, and both coauthors equal for the remaining part.
Part of the research described in this paper is imbedded in COST action FA1206 (STREAM). This work was supported by the Grant No. L001204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I, MEYS. One of us (BZ) owes many thanks to Professor Mirek Strnad for the great hospitality during his stay in the Department of Growth Regulators, Palacky University, Olomouc (CZ).
- Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108:20242–20247. doi: 10.1073/pnas.1111902108 CrossRefPubMedPubMedCentralGoogle Scholar
- Bhattacharya C, Bonfante P, Deagostino A, Kapulnik Y, Larini P, Occhiato EG, Prandi C, Venturello P (2009) A new class of conjugated strigolactone analogues with fluorescent properties: synthesis and biological activity. Org Biomol Chem 7:3413–3420. doi: 10.1039/b907026e CrossRefPubMedGoogle Scholar
- Boyer FD, de Saint GA, Pillot JP, Pouvreau JB, Chen VX, Ramos S, Stévenin A, Simier P, Delavault P, Beau JM, Rameau C (2012) Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol 159:1524–1544. doi: 10.1104/pp.112.195826 CrossRefPubMedPubMedCentralGoogle Scholar
- Boyer FD, de Saint GA, Pouvreau JB, Clavé G, Pillot JP, Roux A, Rasmussen A, Depuydt S, Lauressergues D, Frei Dit Frey N, Heugebaert TS, Stevens CV, Geelen D, Goormachtig S, Rameau C (2014) New strigolactone analogs as plant hormones with low activities in the rhizosphere. Mol Plant 7:675–690. doi: 10.1093/mp/sst163 CrossRefPubMedGoogle Scholar
- Butler LG (1995) Chemical communication between the parasitic weed Striga and its crop host: a new dimension in allelochemistry. In: Inderji K, Einhellig FA (eds), Insights into allelopathy. ACS Symposium Series, ACS Books, Washington, DC, pp 158–168Google Scholar
- Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194. doi: 10.1038/nature07271 CrossRefPubMedGoogle Scholar
- Hu Z, Yamauchi T, Yang J, Jikumaru Y, Tsuchida-Mayama T, Ichikawa H, Takamure I, Nagamura Y, Tsutsumi N, Yamaguchi S, Kyozuka J, Nakazono M (2014) Strigolactone and cytokinin act antagonistically in regulating rice mesocotyl elongation in darkness. Plant Cell Physiol 55:30–41. doi: 10.1093/pcp/pct150 CrossRefPubMedGoogle Scholar
- Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136. doi: 10.1007/s00344-009-9122-7 CrossRefGoogle Scholar
- Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S, Kyozuka J (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135. doi: 10.1093/pcp/pcq083 CrossRefPubMedPubMedCentralGoogle Scholar
- Nefkens GHL, Thuring JWJF, Beenakkers MFM, Zwanenburg B (1997) Synthesis of a phthaloylglycine-derived strigol analogue and is germination stimulatory activity towards seeds of the parasitic weeds Striga hermonthica and Orobanche crenata. J Agric Food Chem 45:2273–2277. doi: 10.1021/jf9604504 CrossRefGoogle Scholar
- Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Mileto I (2011) New potent fluorescent analogues of strigolactones: synthesis and biological activity in parasitic weed germination and fungal branching. Eur J Org Chem 2011:3781–3793. doi: 10.1002/ejoc.201100616 CrossRefGoogle Scholar
- Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:1221–1232. doi: 10.1104/114.240036 CrossRefPubMedPubMedCentralGoogle Scholar
- Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, Li S, Xu TH, Liu Y, Chen RZ, Kovach A, Kang Y, Hou L, He Y, Xie C, Song W, Zhong D, Xu Y, Wang Y, Li J, Zhang C, Melcher K, Xu H (2013) Crystal structures of two phytohormone signal-transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23:436–439. doi: 10.1038/cr.2013.19 CrossRefPubMedPubMedCentralGoogle Scholar
- Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, Ma W, Gao H, Chen J, Yang C, Wang D, Tan J, Zhang X, Guo X, Wang J, Jiang L, Liu X, Chen W, Chu J, Yan C, Ueno K, Ito S, Asami T, Cheng Z, Wang J, Lei C, Zhai H, Wu C, Wang H, Zheng N, Wan J (2013) D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410. doi: 10.1038/nature12878 CrossRefPubMedPubMedCentralGoogle Scholar
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