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Strigolactones (SLs) have been defined as a new group of plant hormones or their derivatives that suppress lateral shoot branching. Recently, a new role for SLs was discovered, in the regulation of root development. Strigolactones were shown to alter root architecture and affect root-hair elongation. Here, I review the recent findings regarding the effects of SLs on root growth and development, and their association with changes in auxin flux. The networking between SLs and other plant hormones that regulate root development is also presented. Strigolactone regulation of plant development suggests that they are coordinators of shoot and root development and mediators of plant responses to environmental conditions.
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However, SLs were known for over 40 yr as germination stimulants of the parasitic plants Striga and Orobanche (Cook et al., 1966; reviewed by Xie et al., 2010) and later, as stimulants of hyphal branching of the symbiotic arbuscular mycorrhizal fungi (reviewed by Xie et al., 2010). Strigolactones are carotenoid-derived terpenoid lactones (Matusova et al., 2005); their presence has been demonstrated in several plant species and in each of these, a mixture of several SL compounds was found (reviewed by Xie et al., 2010).
The roots are the main site of SL biosynthesis in plants, and their synthesis in the lower part of the shoot has also been suggested (reviewed by Dun et al., 2009). Nevertheless, to confer a significant reduction in shoot branching, it is suggested that SLs, their metabolites or other unknown secondary messengers move in the root-to-shoot direction (reviewed by Dun et al., 2009). Accordingly, the SL orobanchol was detected in xylem sap in Arabidopsis, further supporting the suggestion that root-derived SLs are transported to the shoot (Kohlen et al., 2011).
Both SL synthesis and SL signaling mutants have been identified in several plant species. Mutation in carotenoid cleavage dioxygenase (CCD) enzymes (CCD7/MAX3 and CCD8/MAX4) and in MAX1, a cytochrome P450, have been associated with a hyperbranching phenotype and with reduced levels of SLs, suggesting that they catalyse SL biosynthesis (Liang et al., 2010; Vogel et al., 2010; reviewed by Dun et al., 2009; Leyser, 2009). Mutation in MAX2 have been associated with an over-shooting phenotype (Stirnberg et al., 2002), which is not repressed by application of GR24 (a bioactive, synthetic SL; Johnson et al., 1981; Umehara et al., 2008), and is not associated with reduced levels of the SL orobanchol (Kohlen et al., 2011). Moreover, MAX2 has been suggested to be an F-box protein and to function in ubiquitin-mediated degradation of as-yet unknown protein targets (Stirnberg et al., 2007). Hence, MAX2 was suggested to be a component of SL signaling (Umehara et al., 2008).
An additional role in plant development has been recently found for SLs, as modulators of root development. This newly identified role is the focus of this review.
The role of strigolactones in root development
Lateral root formation
Strigolactones were suggested to negatively regulate lateral root (LR) formation in Arabidopsis, under conditions of sufficient phosphate (Pi) nutrition. Mutants deficient in SL biosynthesis (i.e. max3 and max4) and signaling (i.e. max2) were shown to have more LRs than the wild type (WT) (Kapulnik et al., 2011a; Ruyter-Spira et al., 2011). Accordingly, under conditions of sufficient Pi, treatment of seedlings with GR24 led to a reduction in LR formation (Kapulnik et al., 2011a; Ruyter-Spira et al., 2011), whereas under Pi-limiting conditions, SLs led to induction of LR formation (Ruyter-Spira et al., 2011). Both reduction and induction were found in the WT and in the SL-synthesis mutants, but not in the SL-signaling mutant, suggesting that the effect of SL on LR formation is mediated via the MAX2 F-box (Kapulnik et al., 2011a; Ruyter-Spira et al., 2011).
Primary root development
Application of GR24 under favorable growth conditions (sufficient Pi and sugar) led to a MAX2-dependent increase in primary root (PR) length. The opposite effect – inhibition of PR length – was recorded for treatments with relatively higher doses of GR24, in a MAX2-independent fashion. However, under conditions of carbohydrate limitation that usually lead to a reduction in PR length (Jain et al., 2007), GR24 treatments at all concentrations had a positive, MAX2-dependent effect on PR elongation. Accordingly, under conditions of carbohydrate limitation, the PR lengths of SL-deficient and SL-insensitive Arabidopsis plants were shorter than those of WT plants (Ruyter-Spira et al., 2011).
The reduction in PR length in the max plants was accompanied by a reduction in cell number in the PR meristem, which could be rescued by application of GR24 in SL-deficient, but not in SL-insensitive mutants. Hence, it was suggested that SLs are positive regulators of PR elongation, dependent on growth conditions (Ruyter-Spira et al., 2011).
Treatments with GR24 were shown to lead to an increase in root-hair (RH) length in the WT and SL-deficient mutants, but not in the SL-insensitive mutant max2, even when the latter was treated with relatively higher GR24 concentrations. Hence, SLs have a positive effect on RH length, which is mediated via MAX2. This effect of GR24 on RH elongation was evident 24 h after its application, and was reduced under higher doses of GR24 (e.g. 13.5 μM; Kapulnik et al., 2011a).
Taken together, these studies suggest that SLs regulate PR and LR development, as well as RH elongation, thereby affecting plant root development, in addition to shoot development. The differences in SL activity under different sugar and Pi conditions raise the possibility that SLs regulate root development in response to external environmental conditions. However, the use of the synthetic SL GR24 may sometimes be misleading because of its longer stability in water solution compared with natural SLs (Akiyama et al., 2010). Moreover, SL regulation of root development is likely to be conveyed through cross-talk with other phytohormones that regulate PR, LR and RH development. These issues are discussed in more detail in the following.
The networking of strigolactones with other plant hormones during root development
Several studies have suggested that SLs and auxin interact in the shoot: it was further hypothesized that either SL is an auxin-promoted secondary messenger that moves up into the buds to repress their outgrowth (reviewed by Dun et al., 2009), or that SLs mediate a reduction in the shoot’s capacity for polar auxin transport from the apical meristem, thereby leading to inhibition of polar auxin transport from the buds (reviewed by Leyser, 2009). However, studies of SL regulation of root development further broadened and clarified the SL-associated hormonal networks (Fig. 1).
As for the cross-talk between SLs and auxin: on the one hand, auxin has been shown to induce SL synthesis in the root, through induction of MAX3 and MAX4 expression (reviewed by Beveridge & Kyozuka, 2010); on the other, auxin and SLs have been suggested to interact in the regulation of RH, PR and LR development (Kapulnik et al., 2011b; Ruyter-Spira et al., 2011). Strigolactone signaling was shown not to be necessary for the RH elongation induced by auxin, but auxin signaling was shown to enhance the RH elongation response to SLs: the SL-insensitive mutant max2 was responsive to auxin, whereas under low GR24 concentrations, the auxin receptor mutant tir1-1 (Dharmasiri et al., 2005) was less responsive to SLs than the WT (Kapulnik et al., 2011b).
Root-hair elongation is a result of increased auxin levels in the epidermal cells (e.g. Pitts et al., 1998), whereas AUX1-dependent auxin transport through nonhair epidermal cells is necessary for RH elongation (Jones et al., 2009). Hence, it is possible that SLs are involved in RH elongation via modulation of auxin flux, either directly or indirectly (i.e. through modulation of ethylene synthesis, see later for the cross-talk between SLs and ethylene).
Support for the suggestion that SLs mediate auxin flux in the roots, in addition to that in the shoot, comes from several studies. The SLs’ effect on PR growth, cell elongation and RH elongation in tomato was shown, in the presence of exogenously applied auxin, to involve their interference with auxin-efflux carriers (Koltai et al., 2010). Moreover, Ruyter-Spira et al. (2011) found that upon GR24 treatment, PIN1, PIN3 and PIN7-green fluorescent protein (GFP) intensities decrease in the provascular tissue of the PR tip.
Lateral root formation is regulated, among others, by local auxin levels or sensitivity and is dependent, at least in part, on PIN1-auxin efflux activity (reviewed by Péret et al., 2009). Hence, the connection between the effect of SLs on LR formation, auxin level and PIN1 expression was examined. The GR24 treatments resulted in a decrease in PIN1-GFP intensity, suggesting its involvement in the GR24-mediated reduction of LR formation. However, when auxin levels were increased by exogenous application, GR24 application induced, rather than reduced, LR formation, whereas no reduction in PIN1-GFP intensity was seen under these conditions (Ruyter-Spira et al., 2011).
Based on these results, it was suggested that SLs, by being modulators of auxin flux, may alter the auxin optima for LR formation: under relatively low auxin levels, SLs reduce auxin import to the root, leading to inhibition of LR formation, whereas under high auxin levels, this SL-mediated reduction allows the generation of auxin optima, and induction of LR formation (Ruyter-Spira et al., 2011). Under low Pi conditions the changes in root-system architecture were suggested to be a result of increased auxin sensitivity (Pérez-Torres et al., 2008), so it is possible that the effect of SLs on LR formation is conveyed via modulation of local auxin levels or sensitivity, or both. The decreased beta-glucuronidase (GUS) staining derived from the auxin-response reporter DR5-GUS in the aerial parts (i.e. the site of apical auxin production) of GR24-treated plants further supports this suggestion (Ruyter-Spira et al., 2011).
As for the cross-talk between SLs and ethylene: SL signaling was shown to be unnecessary for the RH ethylene response, because the SL-signaling mutant was responsive to ethylene precursor. However, the markedly reduced SL response in the ethylene-signaling mutants etr and ein (Stepanova & Alonso, 2009) suggested that ethylene signaling is involved (although perhaps not exclusively) in the SL response (Kapulnik et al., 2011b). Moreover, blockage of ethylene biosynthesis by the ethylene-synthesis inhibitor 2-aminoethoxyvinylglycine (AVG) abolished the SLs’ effect on RH elongation, whereas root treatment with GR24 elevated transcription of At-ACS2 (Kapulnik et al., 2011b), which encodes one of the key rate-determining enzymes in ethylene biosynthesis (Pech et al., 2010). Together, the results suggest that SLs induce ethylene biosynthesis, that ethylene and SLs are in the same pathway regulating RH elongation, and that ethylene may be epistatic to SLs in this hormonal pathway (Kapulnik et al., 2011b; Fig. 1).
As a result, it might be that ethylene, rather than auxin, is directly involved in the root response to SLs (Fig. 1; Kapulnik et al., 2011b). This can at least be suggested for RH elongation as, on the one hand, ethylene has been shown to regulate auxin synthesis, transport (including auxin efflux and PIN protein expression), response and distribution in the roots (Stepanova & Alonso, 2009 and references therein), and on the other, ethylene has been shown to be epistatic to SLs and its biosynthesis essential for the RH response to SLs (Kapulnik et al., 2011b). Hence, it might be that ethylene, rather than auxin, is directly involved in the RH response to SLs, and that both SL and auxin pathways converge through that of ethylene (Fig. 1; Kapulnik et al., 2011b).
Interestingly, SLs were shown to induce ethylene biosynthesis in seeds of the parasitic plant Striga, leading to seed germination (Sugimoto et al., 2003). This evidence further supports the suggestion that the effect of SLs on RH elongation involves ethylene biosynthesis. Together, the results imply a general SLs on ethylene synthesis, which may affect plant development. However, whether these putative cross-talk junctions between SLs, auxin and ethylene are valid for other types of SL-mediated regulation in plant development remains to be explored.
Strigolactones may be mediators of root responses to the environment
Root hairs elongate in response to growth conditions, and are suggested to be associated with the level of nutrient uptake by the plant. Conditions of nutrient deficiency, including deficiencies in Pi, nitrogen (N) and iron (Fe), lead to RH formation and elongation (reviewed by López-Bucio et al., 2003). Accordingly, RHs are thought to be directly associated with enhancement of the plant’s ability to absorb nutrients from the soil (reviewed by Gilroy & Jones, 2000). It is tempting to speculate that SLs are mediators of the root response to low nutrient conditions: SLs may affect RH elongation and thereby mediate nutrient uptake by the plant.
The development of PRs and LRs has been shown in many studies to be important for plant growth and survival (reviewed by Osmont et al., 2007). Initiation of LR and PR elongation are largely affected by the concentrations of several nutrients, and are regulated by a set of phytohormones (reviewed by Osmont et al., 2007). The Pi status-dependent effect of SLs on LR development found in Arabidopsis (Ruyter-Spira et al., 2011) suggests that the biological role of SLs in roots is regulation of the root’s response to Pi conditions. Support for this suggestion comes from the induction of SL production found under low Pi and low N conditions in several plant species, including Arabidopsis (Yoneyama et al., 2007; López-Ráez et al., 2008; Kohlen et al., 2011); this induction may lead to changes in root development, and thus to a response to growth conditions.
However, the ability of SLs to positively regulate PR elongation under conditions of carbohydrate starvation (Ruyter-Spira et al., 2011) is less easily explained. Conditions of carbohydrate limitation have been reported to lead to a reduction in PR length (Jain et al., 2007). However, the involvement of SLs in this PR response might not be associated with the plant’s response to Pi status, as neither sucrose nor auxin play a role in the determinate growth of PRs exposed to localized Pi deficiency (Jain et al., 2007). It is possible that this positive effect of SLs on PR development is derived from another, unknown mechanism of SL regulation of PR elongation.
As in both rice and Arabidopsis, decreasing Pi concentration in the media leads to increased SL levels in the roots, and to inhibition of tiller or lateral bud outgrowth (Umehara et al., 2010; Kohlen et al., 2011). Therefore, SLs are suggested to be regulators of shoot architecture in response to Pi growth conditions (Umehara et al., 2010; Kohlen et al., 2011). This and their role as regulators of root development, which is growth condition-dependent, suggest that SLs play a pivotal role in plants as modulators of the coordinated development of roots and shoots in response to Pi starvation.
Finally, SLs were initially identified and are known as signaling molecules of plants’ association with parasitic plants and symbiotic arbuscular mycorrhizal fungi (Xie et al., 2010), but it is still unclear whether they evolved to serve as a signal molecule in plant communication, or as hormones for the regulation of plant development. However, the current unveiling of the role of SLs as coordinators of root and shoot development in response to environmental conditions is likely to be crucial for plant survival and productivity, and may have been a major force in SL evolution. It is possible that the primary role of SLs is plant morphogenesis, rather than in plant communication.