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. 2014 Jul 18;166(2):560–569. doi: 10.1104/pp.114.244939

Strigolactone Involvement in Root Development, Response to Abiotic Stress, and Interactions with the Biotic Soil Environment

Yoram Kapulnik 1,*, Hinanit Koltai 1
PMCID: PMC4213088  PMID: 25037210

Strigolactones play a role in root development, root response to nutrient deficiency, and plant interactions in the rhizosphere.

Abstract

Strigolactones, recently discovered as plant hormones, regulate the development of different plant parts. In the root, they regulate root architecture and affect root hair length and density. Their biosynthesis and exudation increase under low phosphate levels, and they are associated with root responses to these conditions. Their signaling pathway in the plant includes protein interactions and ubiquitin-dependent repressor degradation. In the root, they lead to changes in actin architecture and dynamics as well as localization of the PIN-FORMED auxin transporter in the plasma membrane. Strigolactones are also involved with communication in the rhizosphere. They are necessary for germination of parasitic plant seeds, they enhance hyphal branching of arbuscular mycorrhizal fungi of the Glomus and Gigaspora spp., and they promote rhizobial symbiosis. This review focuses on the role played by strigolactones in root development, their response to nutrient deficiency, and their involvement with plant interactions in the rhizosphere.

Strigolactones have been discovered as plant hormones (Gomez-Roldan et al., 2008; Umehara et al., 2008) that are produced by a wide variety of plant species (Xie et al., 2010; Yoneyama et al., 2013). Several different types of strigolactones can be produced by a single plant species, and different varieties of the same plant species may produce mixtures of different types and quantities of strigolactone molecules (Xie et al., 2010; Yoneyama et al., 2013). Strigolactones are also produced in primitive plants, including Embryophyta and Charales (Delaux et al., 2012). In all cases, they are produced and exuded in small amounts (Sato et al., 2003; Yoneyama et al., 2007a, 2007b). Strigolactones are produced primarily in roots, but their biosynthesis is not limited to the root system and also occurs in other plant parts (for review, see Koltai and Beveridge, 2013).

Although strigolactone biosynthesis derives from the carotenoid synthesis pathway (Booker et al., 2004; Matusova et al., 2005), only some of the proteins that are crucial for biosynthesis have been identified to date. In the tested higher plant species, three plastid-localized proteins have been found to be involved in the first stages of strigolactone biosynthesis (Booker et al., 2004, Matusova et al., 2005). One is a carotenoid isomerase DWARF27 (D27), which is characterized in rice (Oryza sativa), Arabidopsis (Arabidopsis thaliana), and pea (Pisum sativum; Lin et al., 2009; Alder et al., 2012; Waters et al., 2012a). It can convert all-trans-β-carotene into 9′-cis-β-carotene (Alder et al., 2012). The latter is then oxidatively tailored, cleaved, and cyclized by two double-bond-specific cleavage enzymes, carotenoid cleavage dioxygenase7 (CCD7) and CCD8 (Booker et al., 2004; Schwartz et al., 2004), resulting in the bioactive strigolactone precursor carlactone (Alder et al., 2012). The conversion of carlactone to strigolactone has not been characterized but may include MORE AXILLARY GROWTH1 (MAX1), a class III cytochrome P450 monooxygenase (Booker et al., 2005; Alder et al., 2012; Cardoso et al., 2014). The presence of CCD enzymes has been shown in several diverse higher plants (Delaux et al., 2012). Moss (Physcomitrella patens) also contains homologs of these three genes and accordingly, can produce strigolactones (Proust et al., 2011). However, only some of these genes are present in other basal plants and algae (Delaux et al., 2012). Approximately 15 strigolactones have been structurally characterized to date (Ruyter-Spira et al., 2013); all consist of an ABC-ring system connected by an enol ether bridge to a butenolide D ring (Xie et al., 2010).

As plant hormones, strigolactones regulate the development of different plant parts. The first indication that strigolactones function as plant hormones came from an examination of hyperbranching mutants. The phenotypes of these mutants could not be attributed to altered levels of or response to one of the established plant hormones known at the time. Hence, a unique signal that was associated with this phenotype was suggested (Beveridge et al., 1997). Later, this signal was identified to be strigolactones and act as a long-distance branching factor that suppresses growth of preformed axillary buds (Gomez-Roldan et al., 2008; Umehara et al., 2008).

Strigolactones dampen auxin transport in the main stem, thereby enhancing competition between axillary branches and restraining axillary bud outgrowth (Bennett et al., 2006; Mouchel and Leyser, 2007; Ongaro and Leyser, 2008; Crawford et al., 2010; Domagalska and Leyser, 2011). Accordingly, strigolactones were shown to act by increasing the rate of removal of PIN-FORMED1 (PIN1), the auxin export protein, from the plasma membrane of xylem parenchyma cells in the stem. This activity was shown by both computational model and experimental data, and it was correlated to the level of shoot branching observed in various mutant combinations and strigolactone treatments (Shinohara et al., 2013). In pea, strigolactones were shown to induce the expression of the bud-specific target gene BRANCHED1, which encodes a transcription factor repressing bud outgrowth (Dun et al., 2012), and be an auxin-promoted secondary messenger (Brewer et al., 2009; Ferguson and Beveridge, 2009; Dun et al., 2012, 2013). Other activities of strigolactone include repression of adventitious root formation (Rasmussen et al., 2012) and plant height (de Saint Germain et al., 2013). They also induce secondary growth in the stem (Agusti et al., 2011). Auxin positively regulates strigolactone biosynthesis by elevating the expression of both MAX3 and MAX4. It has been suggested that auxin and strigolactone modulate each other’s levels and distribution, forming a dynamic feedback loop between the two hormones (Hayward et al., 2009).

As noted, although the main site of strigolactone synthesis is the roots, part of their activity is in the shoot. Therefore, strigolactones are expected to be transported upward in the plant from root to shoot. Evidence to support this suggestion comes from the work by Kohlen et al. (2011), which showed the presence of the strigolactone orobanchol in the xylem sap of Arabidopsis. Another means of strigolactone transport is probably through specific transporters. The petunia (Petunia hybrid) ABC transporter PLEIOTROPIC DRUG RESISTANCE1, localized mainly in the bud/leaf vasculature and subepidermal cells of the root, was identified as a cellular strigolactone exporter. It was shown to regulate the level of symbiosis of arbuscular mycorrhizal fungi (AMF; of the Glomus and Gigaspora spp.; discussed below) and axillary shoot branching (Kretzschmar et al., 2012).

Strigolactones also act in the root to determine root architecture. However, even before strigolactones were identified as plant hormones, they were known to be involved with communication in the rhizosphere. This review focuses on strigolactone activity in the roots as regulators of root system architecture, root hair length, and primary root meristem as well as aspects of their signaling. Their involvement with the root response to nutrient growth conditions will also be presented and discussed. Moreover, the effects of strigolactone on root-rhizosphere communication will be presented along with some implications on strigolactone implementation.

STRIGOLACTONES REGULATE ROOT DEVELOPMENT

One of the first pieces of evidence suggesting that strigolactones have a role in the development of root system architecture was the finding that Arabidopsis mutants in the strigolactone response or biosynthesis have more lateral roots than the wild type (Kapulnik et al., 2011a; Ruyter-Spira et al., 2011). Accordingly, treatment of seedlings with GR24 (a synthetic and biologically active strigolactone; Johnson et al., 1976; Gomez-Roldan et al., 2008; Umehara et al., 2008) repressed lateral root formation in the wild type and the strigolactone-synthesis mutants (max3 and max4) but not in the strigolactone-response mutant (max2), suggesting that the negative effect of strigolactones on lateral root formation is MAX2 dependent (Kapulnik et al., 2011a; Ruyter-Spira et al., 2011). This negative effect on lateral root formation was reversed in Arabidopsis under phosphate deficiency (discussed below; Ruyter-Spira et al., 2011).

Strigolactones are also suggested to regulate primary root length. GR24 led to elongation of the primary root and an increase in meristem cell number in an MAX2-dependent manner (Ruyter-Spira et al., 2011; Koren et al., 2013). Accordingly, under conditions of carbohydrate limitation, a shorter primary root and fewer primary meristem cells were detected in strigolactone-deficient and strigolactone-response mutants compared with the wild type (Ruyter-Spira et al., 2011).

Furthermore, in rice, a major quantitative trait locus on chromosome 1 (qSLB1.1) was identified for the exudation of strigolactones, tillering, and induction of Striga hermonthica germination (Cardoso et al., 2014). Several root architectural traits were mapped in the same region (Topp et al., 2013), suggesting that this locus may be involved in both strigolactone synthesis and root system architecture.

Notably, expression of MAX2 under the SCARECROW (SCR) promoter was sufficient to confer a response to GR24 in an max2-1 mutant background for both lateral root formation and cell number in the primary root meristem (Koren et al., 2013). Because SCR is expressed mainly in the root endodermis and quiescence center (Sabatini et al., 2003), these results point to an important role for the endodermis in strigolactone regulation of root architecture.

Another one of the effects of strigolactones in roots is on root hair length. Exogenous supplementation of various synthetic strigolactone analogs induced root hair elongation in Arabidopsis, the wild type, and the strigolactone-deficient mutants (max3 and max4) but not in the strigolactone-response mutant max2, suggesting that the effect of strigolactones on root hair elongation is mediated by MAX2 (Kapulnik et al., 2011a; Cohen et al., 2013). Furthermore, response to auxin and ethylene signaling is required, at least in part, for the positive effect of strigolactone on root hair elongation. However, MAX2-dependent strigolactone signaling is not necessary for the root hair elongation induced by auxin (Kapulnik et al., 2011b). Hence, strigolactones affect root hair length, at least in part, through the auxin and ethylene pathways (Koltai, 2011). Here too, expression of SCR::MAX2 was sufficient to confer root hair elongation in roots in response to GR24 (Koren et al., 2013). Because root hair elongation is regulated in the epidermis, the sufficiency of MAX2 expression under SCR (expressed mainly in the root endodermis and quiescence center) for GR24 sensitivity suggests that strigolactones act noncell autonomously at short range.

To summarize, strigolactones play a regulatory role in root development. At least part of this activity is performed noncell autonomously and may involve modulation of auxin transport, which is discussed below.

STRIGOLACTONE SIGNALING PATHWAY

As indicated earlier for shoots, in the root, evidence also indicates a role for strigolactones in the regulation of PIN protein activity. One piece of evidence comes from studies of tomato (Solanum lycopersicum) roots, in which exogenous supplementation of 2,4-dichlorophenoxyacetic acid (a synthetic auxin that is not secreted by auxin efflux carriers) led to reversion of the GR24-related root effect, suggesting functional involvement of GR24 with auxin export (Koltai et al., 2010a). Another piece of evidence comes from studies in Arabidopsis, where treatment of seedlings with GR24 led to a decrease in PIN1-GFP intensity in lateral root primordia, suggesting that GR24 regulates PIN1, modulates auxin flux in roots, and as a result, alters the auxin optima necessary for lateral root formation (Ruyter-Spira et al., 2011). Furthermore, in Arabidopsis, after GR24 treatment that leads to root hair elongation, PIN2 polarization was increased in the plasma membrane of the root epidermis in the wild type but not the max2 mutant. In addition, in an MAX2-dependent manner, GR24 treatment led to increased PIN2 endocytosis, increased endosomal movement in the epidermal cells, and changes in actin filament architecture and dynamics (Pandya-Kumar et al., 2014). Together, these results suggest that strigolactones affect plasma membrane localization of PIN proteins. At least for PIN2 in the root, they probably do so by regulating the architecture and dynamics of actin filaments and PIN endocytosis, which are important for PIN2 polarization (Fig. 1; Pandya-Kumar et al., 2014).

Figure 1.

Figure 1.

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A model of the putative signaling pathway of strigolactone in roots. An α/β-fold hydrolase protein may serve as the strigolactone receptor. It may interact with MAX2 and, as a result, lead to degradation by ubiquitination of a repressor (for review, see Waldie et al., 2014). These events or similar events may lead to changes in the architecture and dynamics of actin filaments and PIN endocytosis, which is important for PIN2 polarization. As a result, PIN2 protein polarization is affected, which may lead to changes in auxin flux and execution of strigolactone-associated root effects, such as root hair elongation. SCF, Skp, Cullin, F box.

Upstream of those events are probably those associated with strigolactone reception. One of the components of strigolactone reception was identified several years ago as an F-box protein, MAX2/DWARF3 (D3)/RAMOSUS4 (RMS4) (Stirnberg et al., 2002; Ishikawa et al., 2005; Johnson et al., 2006). An additional component of strigolactone signaling is D14, which is a protein of the α/β-fold hydrolase superfamily (Arite et al., 2009). Petunia DECREASED APICAL DOMINANCE2 (DAD2), a homolog of D14, was shown to interact in a yeast two-hybrid assay with petunia MAX2A only in the presence of GR24, resulting in hydrolysis of GR24 by DAD2 (Hamiaux et al., 2012). In addition, in rice, D14 was shown to bind to GR24 (Kagiyama et al., 2013) and cleave strigolactones (Nakamura et al., 2013).

Moreover, through an Skp, Cullin, F box-containing complex (Moon et al., 2004) and in a D14-dependent and D3-dependent manner, it was shown in rice that strigolactones induce degradation of D53, a class I Chloroplast adenosine 5′-triphosphate protein. D53 acts as a repressor of strigolactone signaling pathway, and its degradation by strigolactones prevents its activity in promoting axillary bud outgrowth (Jiang et al., 2013; Zhou et al., 2013). Furthermore, in Arabidopsis, strigolactones were suggested to induce, in an MAX2-dependent manner, proteasome-mediated degradation of D14 (Chevalier et al., 2014), suggesting a negative regulatory circuit of strigolactones and their own signaling.

This regulatory module of strigolactone/D14-like/D3-like/Skp, Cullin, F box is likely to have been conserved in plant evolution (Waldie et al., 2014). As indicated above, it was shown to be associated with strigolactone-regulated shoot development (Jiang et al., 2013; Zhou et al., 2013). However, it is not clear whether this or a similar reception system acts in the roots (Fig. 1). It might be that diversity in this module confers tissue specificity. Different D14-like proteins attached to D3/MAX2 may confer different substrate specificity and as a result, a specific effect on plant development. For example, a KARRIKIN-INSENSITIVE2 (D14-LIKE) -MAX2-dependent pathway is responsible for regulating seed germination, seedling growth, and leaf and rosette development in response to karrikins, which are strigolactone-analogous compounds originally found in forest fire smoke (Flematti et al., 2004; Nelson et al., 2011; Waters et al., 2012b, 2014). Modules for strigolactone response that are composed of other α/β-fold hydrolases and/or degradation of other repressors could potentially lead to execution of the strigolactone-related processes in roots (Fig. 1).

STRIGOLACTONES ARE INVOLVED IN ROOT RESPONSES TO ABIOTIC STRESS CONDITIONS

Strigolactones seem to have been involved in plant responses to environmental stimuli from their early evolution. In moss, they determine the patterns of growth and responses between neighboring colonies (Proust et al., 2011). In higher plants, they are involved in both shoot and root architecture in response to nutritional conditions.

The inorganic form of phosphorus (Pi) that is available to plants is an essential macronutrient for growth and development, and in many places, it is considered to be a limiting factor for growth (Bieleski, 1973; Maathuis, 2009). To cope with Pi deprivation, plants modify their growth pattern and architecture. The shoot-to-root ratio is reduced under these conditions (McCain and Davies, 1983); shoot branching is inhibited (for review, see Domagalska and Leyser, 2011), and root architecture is altered (López-Bucio et al., 2003; Osmont et al., 2007). Elongation of the primary root is inhibited under conditions of Pi deficiency (Sánchez-Calderón et al., 2005), and lateral root development is promoted (Nacry et al., 2005), probably for increased foraging of subsurface soil. After extended deprivation, root growth is also inhibited (Nacry et al., 2005). It should be noted, however, that these general patterns are not identical in all plant species. For example, under Pi deprivation, primary root growth is inhibited in some Arabidopsis ecotypes but not in others (Chevalier et al., 2003).

Several plant hormones are known to regulate root system architecture in response to nutrient conditions. For example, under low Pi conditions, the changes in lateral root formation in Arabidopsis have been suggested to result from increased auxin sensitivity mediated by an increase in the expression of the auxin receptor TRANSPORT INHIBITOR RESPONSE1 (TIR1; Pérez-Torres et al., 2008). Strigolactones might be another plant hormone involved in the regulation of root system architecture in response to nutrient conditions. Although under conditions of sufficient Pi, strigolactones negatively regulate lateral root formation (Kapulnik et al., 2011a), they reverse their effect to positive regulation when Pi is limited (Ruyter-Spira et al., 2011). This suggests that strigolactones act as another key regulator of lateral root formation, promoting their development under low Pi conditions and repressing their emergence once Pi is abundant.

The length and density of root hairs are increased under Pi-deficient conditions, probably to expand root surface area and enhance nutrient acquisition (Bates and Lynch, 2000; Gilroy and Jones, 2000; Péret et al., 2011). Indeed, the plant’s ability to absorb nutrients from the soil is suggested to be directly associated with root hair length and number (for review, see Gilroy and Jones, 2000; Sánchez-Calderón et al., 2005). The recorded ability of strigolactone analogs to increase root hair length (Kapulnik et al., 2011a) may indicate their role in root hair elongation as an adaptive process in plants to growth conditions.

Also of significance is the dependence on strigolactones for the seedling response to Pi deprivation in terms of increasing root hair density. Arabidopsis mutants, defective in strigolactone biosynthesis or response, have a reduced ability to increase their root hair density in response to low Pi shortly after germination (Mayzlish-Gati et al., 2012). In accordance with the suggestion that low Pi response is mediated by an increase in TIR1 expression (Pérez-Torres et al., 2008), the strigolactone-response mutant, under conditions of Pi deprivation, displayed a reduction rather than induction of TIR1 expression (Mayzlish-Gati et al., 2012).

The reduced ability of strigolactone mutants to respond to low Pi conditions shortly after germination (Mayzlish-Gati et al., 2012) may compromise survival of these seedlings under these conditions. These findings suggest an important role for strigolactones in plant adaptation to stress. However, later in plant development, even the strigolactone max2 mutant recovers and is able to respond to low Pi conditions (Mayzlish-Gati et al., 2012). This seedling recovery suggests the involvement of other mechanisms that are not dependent on strigolactones for responding to Pi deprivation, which are effective later in plant development.

Similarly, strigolactone involvement in responses to phosphate and nitrate (NO3−) was shown in rice by analyzing the response of strigolactone biosynthesis (d10 and d27) or strigolactone-insensitive (d3) mutants to reduced concentrations of Pi or NO3−. Reduced Pi or NO3− concentrations led to increased seminal root length and decreased lateral root density in the wild type but not the strigolactone mutants. Application of GR24 restored seminal root length and lateral root density in the wild type and the strigolactone-biosynthesis mutants but not the strigolactone-response mutant, suggesting that strigolactones are involved with the response to Pi and NO3− in rice as well, leading to a D3-dependent change in rice root growth. In addition, based on changes in the transport of radiolabeled indole-3-acetic acid, it was suggested that the mechanisms underlying this regulatory role of D3/strigolactones involve modulation of auxin transport from shoots to roots (Sun et al., 2014).

Pi deprivation leads to an increase in strigolactone exudation. Nitrogen deficiency has also been shown to increase strigolactone exudation. Nevertheless, it might be that nitrogen deficiency affects strigolactone levels through its effect on phosphate levels in the shoot. Indeed, a correlation was found between shoot Pi levels and strigolactone exudation across plant species (Yoneyama et al., 2007a, 2007b, 2012). A clear correlation was also found in both Arabidopsis and rice between this elevation in strigolactone levels and a decrease in shoot branching under restricted Pi growth conditions. In Arabidopsis, in correlation with the changes in shoot architecture, the level of the strigolactone orobanchol in the xylem sap was increased under Pi deficiency (Kohlen et al., 2011). In rice, under these conditions, tiller bud outgrowth was inhibited, and root strigolactone (2′-epi-5-deoxystrigol) levels increased (Umehara et al., 2008). The increase in strigolactone biosynthesis and exudation under low Pi conditions may also induce increased branching of mycorrhizal hyphae (detailed below; Akiyama et al., 2005; Besserer et al., 2006, 2008; Gomez-Roldan et al., 2008; Yoneyama et al., 2008) and hence, possibly, increased mycorrhization.

STRIGOLACTONES ARE SIGNALS FOR PLANT INTERACTIONS

Strigolactones were initially identified as germination stimulants of the parasitic plants Striga spp. and broomrape (Orobanche spp.; Cook et al., 1972; Yokota et al., 1998; Matusova et al., 2005; Xie et al., 2007, 2008a, 2008b, 2009; Goldwasser et al., 2008; Gomez-Roldan et al., 2008). It was only later that strigolactones were also identified as stimulants of hyphal branching in AMF (Akiyama et al., 2005; Besserer et al., 2006, 2008; Gomez-Roldan et al., 2008; Yoneyama et al., 2008). In addition, strigolactones were shown to stimulate nodulation (Nod) in the legume-rhizobium interaction process (Soto et al., 2010; Foo and Davies, 2011).

Mycorrhizal Symbiosis

The most prevalent symbiosis on earth is the arbuscular mycorrhizal (AM) symbiosis, which consists of an association between the roots of higher plants and soil AMF. The AMF are members of the fungal phylum Glomeromycota (Redecker and Raab, 2006), and symbiotic associations are formed with most terrestrial vascular flowering plants (Smith and Read, 2008), in most cases contributing to plant development, especially under suboptimal growth conditions. During the symbiosis, AMF hyphae, which extend through the soil, provide a greater root surface area to exploit a larger volume of soil, thereby enhancing the amount of nutrients absorbed from the soil for the plant (Rausch and Bucher, 2002). In return, the fungus receives fixed carbon in the form of Glc (for review, see Douds et al., 2000), hexoses (Shachar-Hill et al., 1995; Solaiman and Saito, 1997), or Suc from the host.

In general, the AM symbiosis is comprised of two distinct functional stages: the presymbiotic stage and the symbiotic stage. A very detailed description of the presymbiotic stage confirmed that fungal spore germination in the soil and the growth of fungal hyphae are both stimulated in the presence of a host root (Mosse and Hepper, 1975; Gianinazzi-Pearson and Gianinazzi, 1989; Giovannetti et al., 1996; Buée et al., 2000; Nagahashi and Douds, 2000; Requena et al., 2007). These two phenomena, together with the hyphal branching response, may reflect unique communication in the rhizosphere to enhance successful mycorrhization on the host (Koske and Gemma, 1992).

Purified strigolactones from root exudates or synthetic strigolactones have been shown to be capable of inducing hyphal branching in many AMF (Akiyama et al., 2005). These molecules are present at subnanogram levels in the rhizosphere (Akiyama et al., 2005; Akiyama and Hayashi, 2006). Similarly, the synthetic strigolactone GR24 was shown to effectively induce AMF hyphal branching at a concentration of 10−8 m (Gomez-Roldan et al., 2008). Accordingly, strigolactone-deficient mutants of pea and tomato exhibit reduced levels of AMF hyphal branching in their rhizosphere compared with the response obtained in the presence of wild-type root exudates (Gomez-Roldan et al., 2008; Koltai et al., 2010b).

In a more in-depth study, it was shown that strigolactones rapidly induce changes in AMF energy metabolism before any gene expression process in the fungus can be detected. When AMF hyphae were exposed to the synthetic strigolactone GR24, a rapid alteration (within 60 min) in mitochondrial shape, density, and motility was observed. In the AMF Gigaspora rosea hyphae, NADH concentrations, dehydrogenase activity, and ATP content were altered within minutes by application of GR24 (Besserer et al., 2006; 2008).

The importance of strigolactones to AMF establishment was reinforced by the observation of a lower colonization rate of a tomato strigolactone biosynthesis mutant by AMF spores than that obtained in wild-type roots. Interestingly, these differences were less pronounced when plants were inoculated with whole inoculum (consisting of spores, hyphae, and infected roots; Koltai et al., 2010b).

Nevertheless, it was shown that root exudates of mycorrhitic plants induce Striga spp. and Orobanche spp. seed germination to a lesser extent than the induction obtained by exudates of nonmycorrhitic plants (Lendzemo et al., 2009; Fernández-Aparicio et al., 2010). Moreover, strigolactone production was shown to be significantly reduced in roots of mycorrhitic tomato plants (López-Ráez et al., 2011). Therefore, strigolactones may be negatively regulated by AMF through a feedback loop. Alternatively, it may be that AMF colonization has a significant impact on enhancement of AM symbiosis and consequently, increased Pi acquisition, which may then be reflected in elevated levels of phosphate content, the latter inducing suppression of strigolactone biosynthesis.

It is not yet clear whether strigolactones have any role during fungal morphogenesis in the host cortical cells or symbiosis stages. Moreover, it is not clear whether strigolactones are essential for the AMF interaction.

Parasitic Plants

Witchweed (Striga spp.) and broomrape (Orobanche spp. and Phelipanche spp.) are important parasitic weeds that have a devastating effect on the production of many crop species, resulting in economic damage and food losses worldwide (Parker, 2009). The damage conferred on crop development and productivity has been summarized elsewhere (Joel, 2000; Gressel and Joel, 2013).

The communication between parasites and their host plants depends on strigolactones as signal molecules that are exuded from the host roots into the rhizosphere. These signals mostly involve induction of seed germination of the parasitic plants, which within a few days, must attach to their host to acquire nutrients or die (Joel and Bar, 2013). This communication allows germination of the parasitic plant at the right distance from the root surface, at the right time in the season, and with the right nutritional, temperature, and moisture levels in the host rhizosphere. After the parasitic plant’s germination, a tubercle develops underground, and shoot outgrowth is initiated. The shoots emerge above the ground, flower, and produce tens of thousands of seeds (for review, see Joel, 2013).

Three types of isoprenoid compounds stimulate the germination of root parasitic plants: dihydrosorgoleone, sesquiterpene lactones, and strigolactones (Bouwmeester et al., 2003). Strigolactones are active at extremely low concentrations (on the order of 10−7–10−15 m; Joel, 2000). A variety of natural strigolactones were shown to be able to induce germination of Orobanche minor from 10 pm strigolactones (for orobanchol, 2'-epiorobanchol, and sorgomol) to 10 nm for 7-oxoorobanchol. The synthetic analog GR24 is 100-fold less active than natural strigolactones (Kim et al., 2010). Advances in chromatography and mass spectrometry are enabling the discovery and characterization of novel strigolactones.

Symbiotic Interactions with Rhizobium spp.

The nitrogen-fixing bacteria of the genus Rhizobium spp. play a fundamental role in nodule formation and beneficial symbiotic interactions on the roots of legumes, such as pea, bean (Phaseolus vulgaris), clover (Trifolium spp.), and alfalfa (Medicago sativa). The symbiotic interaction involves signal exchange between the partners that leads to mutual recognition and development of the nodule structure. In short, at the preinfection stage, the bacteria sense flavonoids that are secreted from the legume host roots. These flavonoid molecules, which are specific to each legume-rhizobium interaction, activate the production and secretion of lipochitooligosaccharide Nod factors from the bacteria that are recognized by the host plant. In most cases, Nod-factor perception leads to induction of a cascade of signaling events, such as root hair deformation and infection thread formation, and is involved in triggering cell division in the cortex of the root, leading to nodule organ formation. Production of Nod factors and exopolysaccharides by many of the rhizobium bacteria elicits an infection thread, where the penetrated bacteria multiply. Intracellular bacterial cells then differentiate to bacteroids (the nitrogen-fixing stage of the symbiosis). In addition to the morphological and cellular modifications, plants and bacteria produce and respond to large groups of peptides, transcriptional factors, and early and late Nod genes. However, the molecular mechanisms by which many of them are involved in the differentiation process are poorly understood. Within the nodule meristem and after cell differentiation, rhizobia bacteroids supply ammonia or amino acids to the plant and in return, receive organic acids as a carbon and energy source (Markmann and Parniske, 2009).

The ability of strigolactones to alter plant meristem development led to the search for strigolactone involvement in this symbiotic interaction. The potential of strigolactones to control nodulation was verified using the strigolactone-deficient rms1 mutant in pea (Foo and Davies, 2011). This work showed that endogenous strigolactones are positive regulators of nodulation in this plant. Using rms1 mutant root exudates and root tissue that were almost completely deficient in strigolactones, Foo and Davies (2011) showed a 40% reduction in the number of nodules relative to wild-type plants that contained strigolactones. Application of GR24 to rms1 plants resulted in an increase in the number of nodules on the mutant roots to the level obtained on the wild type (without exogenous application of strigolactones). GR24 application can also enhance nodule number in wild-type pea, alfalfa, and Lotus japonicus (Soto et al., 2010; Foo and Davies, 2011; Liu et al., 2013). It was also shown that strigolactones in the root but not shoot-derived factors can regulate nodule number (Foo et al., 2014). Genetic studies indicated that strigolactones may act relatively early in nodule formation rather than during nodule organogenesis (Foo et al., 2013a, 2013b). Moreover, it was shown that strigolactones do not influence nodulation by acting directly on the rhizobium bacteria (Soto et al., 2010) or the calcium signaling that follows flavonoid perception (Moscatiello et al., 2010). It was suggested that strigolactones are not essential for the development of a functional nodule but may be important in determining the optimal nodule number, thereby having a quantitative effect on nodulation in pea (Foo et al., 2014).

The mechanism governing strigolactone enhancement of the nodulation process is still an enigma. One potential explanation might be that strigolactones interact with auxin distribution during the cell division process that leads to nodule development. Auxin was found to be accumulated in dividing cortical cells in L. japonicas, and NODULE INCEPTION, a key transcription factor in nodule development, was found to positively regulate this accumulation (Suzaki et al., 2012). Thus, the fact that strigolactones also regulate auxin pathways and that auxin positively regulates strigolactone production (Hayward et al., 2009), suggests an additional regulatory path for this symbiotic interaction as a positive feedback regulation loop between auxin and strigolactones in the promotion of nodulation in legume roots.

CONCLUDING REMARKS

Strigolactones are an important group of molecules. They likely developed in plants as key regulators of plants’ developmental adaptations to environmental conditions. Their production and exudation from roots were used by other organisms to the benefit (AMF and rhizobia) or detriment (parasitic plants) of the host plants. Strigolactones may be involved in additional cases of communication in the rhizosphere as well as additional responses of the plant to growth conditions. This is because of the high complexity of the rhizosphere (Jones and Hinsinger, 2008), which is composed of (1) a multiplicity of organisms and (2) microconditions in soil pockets (e.g. low levels of nutrients). This complexity may hinder the evaluation of additional functions of strigolactones under the nonhomogeneous rhizospheric conditions that are normally found in nature.

Another interesting aspect of strigolactones is their potential use in agriculture. A number of publications have discussed their implementation as inducers of suicidal seed germination of parasitic plant (Zwanenburg et al., 2009, 2013; Vurro and Yoneyama, 2012). However, strigolactones may be used in additional approaches for the development of new agricultural methodologies and technologies compatible with emerging concepts of sustainable agriculture. For example, strigolactones may be used for improvement of root system architecture (e.g. to develop a hyperbranched root system for increased nutrient use efficiency or deeper roots for increased water use efficiency). They may also be used for regulation of shoot branching when, for example, the emergence of axillary branches is undesirable. Strigolactone analogs and mimics that are specific for one activity (e.g. shoot branching) are already being developed (Fukui et al., 2011, 2013; Boyer et al., 2014). Strigolactone inhibitors may be used to enhance rooting of plant cuttings (Rasmussen et al., 2012), potentially promoting the propagation of woody plants for the industry and conservation of endangered species. Today's new strigolactone analogs and mimics, which are under development or being synthesized (Zwanenburg et al., 2009; Prandi et al., 2011), are likely to substantially promote the ability to use strigolactones to the benefit of agriculture.

Glossary

AM

arbuscular mycorrhizal

AMF

arbuscular mycorrhizal fungi

NO3−

nitrate

Nod

nodulation

Pi

inorganic form of phosphorus

References

  1. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, et al. (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108: 20242–20247 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akiyama K, Hayashi H. (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot (Lond) 97: 925–931 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akiyama K, Matsuzaki K, Hayashi H. (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827 [DOI] [PubMed] [Google Scholar]
  4. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S. (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348–1351 [DOI] [PubMed] [Google Scholar]
  5. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J. (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50: 1416–1424 [DOI] [PubMed] [Google Scholar]
  6. Bates TR, Lynch JP. (2000) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87: 964–970 [PubMed] [Google Scholar]
  7. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O. (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16: 553–563 [DOI] [PubMed] [Google Scholar]
  8. Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N. (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148: 402–413 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N. (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4: e226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Beveridge CA, Symons GM, Murfet IC, Ross JJ, Rameau C. (1997) The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol 115: 1251–1258 [Google Scholar]
  11. Bieleski RL. (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24: 225–252 [Google Scholar]
  12. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O. (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14: 1232–1238 [DOI] [PubMed] [Google Scholar]
  13. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O. (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8: 443–449 [DOI] [PubMed] [Google Scholar]
  14. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH. (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6: 358–364 [DOI] [PubMed] [Google Scholar]
  15. Boyer FD, de Saint Germain A, Pouvreau JB, Clavé G, Pillot JP, Roux A, Rasmussen A, Depuydt S, Lauressergues D, Frei Dit Frey N, et al. (2014) New strigolactone analogs as plant hormones with low activities in the rhizosphere. Mol Plant 7: 675–690 [DOI] [PubMed] [Google Scholar]
  16. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA. (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150: 482–493 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G. (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13: 693–698 [DOI] [PubMed] [Google Scholar]
  18. Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO, Meharg C, Wright MH, Liu J, Meng X, et al. (2014) Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci USA 111: 2379–2384 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Chevalier F, Nieminen K, Sánchez-Ferrero JC, Rodríguez ML, Chagoyen M, Hardtke CS, Cubas P. (2014) Strigolactone promotes degradation of DWARF14, an α/β hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26: 1134–1150 [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Chevalier F, Pata M, Nacry P, Doumas P, Rossignol M. (2003) Effects of phosphate availability on the root system architecture: large‐scale analysis of the natural variation between Arabidopsis accessions. Plant Cell Environ 26: 1839–1850 [Google Scholar]
  21. Cohen M, Prandi C, Occhiato EG, Tabasso S, Wininger S, Resnick N, Steinberger Y, Koltai H, Kapulnik Y. (2013) Structure-function relations of strigolactone analogs: activity as plant hormones and plant interactions. Mol Plant 6: 141–152 [DOI] [PubMed] [Google Scholar]
  22. Cook CE, Whichard LP, Wall M, Egley GH, Coggon P, Luhan PA, McPhail AT. (1972) Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J Am Chem Soc 94: 6198–6199 [Google Scholar]
  23. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O. (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905–2913 [DOI] [PubMed] [Google Scholar]
  24. de Saint Germain A, Ligerot Y, Dun EA, Pillot JP, Ross JJ, Beveridge CA, Rameau C. (2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol 163: 1012–1025 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G, Séjalon-Delmas N. (2012) Origin of strigolactones in the green lineage. New Phytol 195: 857–871 [DOI] [PubMed] [Google Scholar]
  26. Domagalska MA, Leyser O. (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12: 211–221 [DOI] [PubMed] [Google Scholar]
  27. Douds DD, Jr, Pfeffer PE, Shachar-Hill Y. (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In Kapulnik Y, Douds DD, Jr, eds, Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 107–130 [Google Scholar]
  28. Dun EA, de Saint Germain A, Rameau C, Beveridge CA. (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158: 487–498 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Dun EA, de Saint Germain A, Rameau C, Beveridge CA. (2013) Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 6: 128–140 [DOI] [PubMed] [Google Scholar]
  30. Ferguson BJ, Beveridge CA. (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149: 1929–1944 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Fernández-Aparicio M, García-Garrido JM, Ocampo JA, Rubiales D. (2010) Colonisation of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche species seed germination. Weed Res 50: 262–268 [Google Scholar]
  32. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD. (2004) A compound from smoke that promotes seed germination. Science 305: 977. [DOI] [PubMed] [Google Scholar]
  33. Foo E, Davies NW. (2011) Strigolactones promote nodulation in pea. Planta 234: 1073–1081 [DOI] [PubMed] [Google Scholar]
  34. Foo E, Ferguson BJ, Reid JB. (2014) The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway. Ann Bot (Lond) 113: 1037–1045 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Foo E, Yoneyama K, Hugill C, Quittenden LJ, Reid JB. (2013a) Strigolactones: internal and external signals in plant symbioses? Plant Signal Behav 8: e23168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB. (2013b) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6: 76–87 [DOI] [PubMed] [Google Scholar]
  37. Fukui K, Ito S, Asami T. (2013) Selective mimics of strigolactone actions and their potential use for controlling damage caused by root parasitic weeds. Mol Plant 6: 88–99 [DOI] [PubMed] [Google Scholar]
  38. Fukui K, Ito S, Ueno K, Yamaguchi S, Kyozuka J, Asami T. (2011) New branching inhibitors and their potential as strigolactone mimics in rice. Bioorg Med Chem Lett 21: 4905–4908 [DOI] [PubMed] [Google Scholar]
  39. Gianinazzi-Pearson V, Gianinazzi S. (1989) Cellular and genetical aspects of interactions between hosts and fungal symbionts in mycorrhizae. Genome 31: 336–341 [Google Scholar]
  40. Gilroy S, Jones DL. (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5: 56–60 [DOI] [PubMed] [Google Scholar]
  41. Giovannetti M, Sbrana C, Citernesi AS, Avio L. (1996) Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New Phytol 133: 65–71 [Google Scholar]
  42. Goldwasser Y, Yoneyama K, Xie X, Yoneyama K. (2008) Production of Strigolactones by Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant Growth Regul 55: 21–28 [Google Scholar]
  43. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, et al. (2008) Strigolactone inhibition of shoot branching. Nature 455: 189–194 [DOI] [PubMed] [Google Scholar]
  44. Gressel J, Joel DM. (2013) Weedy orobanchaceae: the problem. In Joel DM, Gressel J, Musselman LJ, eds, Parasitic Orobanchaceae. Springer, Berlin, pp 309–312 [Google Scholar]
  45. Hamiaux C, Drummond RSM, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC. (2012) DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22: 2032–2036 [DOI] [PubMed] [Google Scholar]
  46. Hayward A, Stirnberg P, Beveridge C, Leyser O. (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151: 400–412 [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J. (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46: 79–86 [DOI] [PubMed] [Google Scholar]
  48. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, et al. (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401–405 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Joel DM. (2000) The long-term approach to parasitic weeds control: manipulation of specific developmental mechanisms of the parasite. Crop Prot 19: 753–758 [Google Scholar]
  50. Joel DM. (2013) The haustorium and the life cycles of parasitic orobanchaceae. In Joel DM, Gressel J, Musselman LJ, eds, Parasitic Orobanchaceae. Springer, Berlin, pp 21–23 [Google Scholar]
  51. Joel DM, Bar H. (2013) The seed and the seedling. In Joel DM, Gressel J, Musselman LJ, eds, Parasitic Orobanchaceae. Springer, Berlin, pp 147–165 [Google Scholar]
  52. Johnson AW, Rosebery G, Parker C. (1976) A novel approach to Striga and Orobanche control using synthetic germination stimulants. Weed Res 16: 223–227 [Google Scholar]
  53. Johnson X, Brcich T, Dun EA, Goussot M, Haurogné K, Beveridge CA, Rameau C. (2006) Branching genes are conserved across species: Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142: 1014–1026 [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Jones D, Hinsinger P. (2008) The rhizosphere: complex by design. Plant Soil 312: 1–6 [Google Scholar]
  55. Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, Yamaguchi S, Hakoshima T. (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 18: 147–160 [DOI] [PubMed] [Google Scholar]
  56. Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier JP, Bécard G, Belausov E, et al. (2011a) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233: 209–216 [DOI] [PubMed] [Google Scholar]
  57. Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H. (2011b) Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J Exp Bot 62: 2915–2924 [DOI] [PubMed] [Google Scholar]
  58. Kim HI, Xie X, Kim HS, Chun JC, Yoneyama K, Nomura T, Takeuchi Y, Yoneyama K. (2010) Structure-activity relationship of naturally occurring strigolactones in Orobanche minor seed germination stimulation. J Pestic Sci 35: 344–347 [Google Scholar]
  59. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C. (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155: 974–987 [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Koltai H. (2011) Strigolactones are regulators of root development. New Phytol 190: 545–549 [DOI] [PubMed] [Google Scholar]
  61. Koltai H, Beveridge CA. (2013) Strigolactones and the coordinated development of shoot and root. In Baluška F, ed, Long-Distance Systemic Signaling and Communication in Plants. Springer, Berlin, pp 189–204 [Google Scholar]
  62. Koltai H, Dor E, Hershenhorn J, Joel D, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, et al. (2010a) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29: 129–136 [Google Scholar]
  63. Koltai H, LekKala SP, Bhattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E, Yoneyama K, Yoneyama K, Hershenhorn J, et al. (2010b) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61: 1739–1749 [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Koren D, Resnick N, Mayzlish Gati E, Belausov E, Weininger S, Kapulnik Y, Koltai H. (2013) Strigolactone signaling in the endodermis is sufficient to restore root responses and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol 198: 866–874 [DOI] [PubMed] [Google Scholar]
  65. Koske RE, Gemma JN. (1992) Fungal reactions to plants prior to mycorrhizal formation. In Allen MF, ed, Mycorrhizal Functioning: An Integrative Plant-Fungal Process. Chapman & Hall, New York, pp 3–36 [Google Scholar]
  66. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E. (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483: 341–344 [DOI] [PubMed] [Google Scholar]
  67. Lendzemo V, Kuyper TW, Vierheilig H. (2009) Striga seed-germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi. Mycorrhiza 19: 287–294 [DOI] [PubMed] [Google Scholar]
  68. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, et al. (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512–1525 [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F. (2013) Carotenoid cleavage dioxygenase 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64: 1967–1981 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L. (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280–287 [DOI] [PubMed] [Google Scholar]
  71. López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ. (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168: 294–297 [DOI] [PubMed] [Google Scholar]
  72. Maathuis FJM. (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12: 250–258 [DOI] [PubMed] [Google Scholar]
  73. Markmann K, Parniske M. (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14: 77–86 [DOI] [PubMed] [Google Scholar]
  74. Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ. (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139: 920–934 [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y, et al. (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160: 1329–1341 [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. McCain S, Davies MS. (1983) Effects of pretreatment with phosphate in natural populations of Agrostis capillaris L. New Phytol 94: 367–379 [Google Scholar]
  77. Moon J, Parry G, Estelle M. (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16: 3181–3195 [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Moscatiello R, Squartini A, Mariani P, Navazio L. (2010) Flavonoid-induced calcium signalling in Rhizobium leguminosarum bv. viciae. New Phytol 188: 814–823 [DOI] [PubMed] [Google Scholar]
  79. Mosse B, Hepper C. (1975) Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5: 215–223 [Google Scholar]
  80. Mouchel CF, Leyser O. (2007) Novel phytohormones involved in long-range signaling. Curr Opin Plant Biol 10: 473–476 [DOI] [PubMed] [Google Scholar]
  81. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P. (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138: 2061–2074 [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Nagahashi G, Douds DD., Jr (2000) Partial separation of root exudate components and their effects upon the growth of germinated spores of AM fungi. Mycol Res 104: 1453–1464 [Google Scholar]
  83. Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X, Ito E, Ito S, Park SH, et al. (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4: 2613. [DOI] [PubMed] [Google Scholar]
  84. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM. (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108: 8897–8902 [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Ongaro V, Leyser O. (2008) Hormonal control of shoot branching. J Exp Bot 59: 67–74 [DOI] [PubMed] [Google Scholar]
  86. Osmont KS, Sibout R, Hardtke CS. (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58: 93–113 [DOI] [PubMed] [Google Scholar]
  87. Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H, Belausov E, Wininger S, Abu-Abied M, Kapulnik Y, et al. (2014) Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol 202: 1184–1196 [DOI] [PubMed] [Google Scholar]
  88. Parker C. (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65: 453–459 [DOI] [PubMed] [Google Scholar]
  89. Péret B, Clément M, Nussaume L, Desnos T. (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16: 442–450 [DOI] [PubMed] [Google Scholar]
  90. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L. (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20: 3258–3272 [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Miletto 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 [Google Scholar]
  92. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F, Rameau C. (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531–1539 [DOI] [PubMed] [Google Scholar]
  93. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, et al. (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158: 1976–1987 [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Rausch C, Bucher M. (2002) Molecular mechanisms of phosphate transport in plants. Planta 216: 23–37 [DOI] [PubMed] [Google Scholar]
  95. Redecker D, Raab P. (2006) Phylogeny of the glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers. Mycologia 98: 885–895 [DOI] [PubMed] [Google Scholar]
  96. Requena N, Serrano E, Ocón A, Breuninger M. (2007) Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68: 33–40 [DOI] [PubMed] [Google Scholar]
  97. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H. (2013) The biology of strigolactones. Trends Plant Sci 18: 72–83 [DOI] [PubMed] [Google Scholar]
  98. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, et al. (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155: 721–734 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Sabatini S, Heidstra R, Wildwater M, Scheres B. (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17: 354–358 [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L. (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46: 174–184 [DOI] [PubMed] [Google Scholar]
  101. Sato D, Awad AA, Chae SH, Yokota T, Sugimoto Y, Takeuchi Y, Yoneyama K. (2003) Analysis of strigolactones, germination stimulants for striga and orobanche, by high-performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 51: 1162–1168 [DOI] [PubMed] [Google Scholar]
  102. Schwartz SH, Qin X, Loewen MC. (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279: 46940–46945 [DOI] [PubMed] [Google Scholar]
  103. Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG. (1995) Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiol 108: 7–15 [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Shinohara N, Taylor C, Leyser O. (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e1001474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Smith S, Read D, editors (2008) Mycorrhizal Symbiosis, Ed 3. Academic Press Elsevier, New York [Google Scholar]
  106. Solaiman MZ, Saito M. (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol 136: 533–538 [DOI] [PubMed] [Google Scholar]
  107. Soto MJ, Fernandez-Aparicio MN, Castellanos-Morales V, Garcia-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H. (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42: 383–385 [Google Scholar]
  108. Stirnberg P, van De Sande K, Leyser HMO. (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131–1141 [DOI] [PubMed] [Google Scholar]
  109. Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G. (March 4, 2014) Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M. (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139: 3997–4006 [DOI] [PubMed] [Google Scholar]
  111. Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee CR, Zurek PR, Symonova O, Zheng Y, Bucksch A, Mileyko Y, Galkovskyi T, et al. (2013) 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. Proc Natl Acad Sci USA 110: E1695–E1704 [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, et al. (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195–200 [DOI] [PubMed] [Google Scholar]
  113. Vurro M, Yoneyama K. (2012) Strigolactones—intriguing biologically active compounds: perspectives for deciphering their biological role and for proposing practical application. Pest Manag Sci 68: 664–668 [DOI] [PubMed] [Google Scholar]
  114. Waldie T, McCulloch H, Leyser O. (February 25, 2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 10.1111/tpj.12488 [DOI] [PubMed] [Google Scholar]
  115. Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA. (2012a) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol 159: 1073–1085 [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM. (2012b) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139: 1285–1295 [DOI] [PubMed] [Google Scholar]
  117. Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM. (January 16, 2014) The karrikin response system of Arabidopsis. Plant J 10.1111/tpj.12488 [DOI] [PubMed] [Google Scholar]
  118. Xie X, Kusumoto D, Takeuchi Y, Yoneyama K, Yamada Y, Yoneyama K. (2007) 2′-epi-orobanchol and solanacol, two unique strigolactones, germination stimulants for root parasitic weeds, produced by tobacco. J Agric Food Chem 55: 8067–8072 [DOI] [PubMed] [Google Scholar]
  119. Xie X, Yoneyama K, Harada Y, Fusegi N, Yamada Y, Ito S, Yokota T, Takeuchi Y, Yoneyama K. (2009) Fabacyl acetate, a germination stimulant for root parasitic plants from Pisum sativum. Phytochemistry 70: 211–215 [DOI] [PubMed] [Google Scholar]
  120. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Takeuchi Y, Sugimoto Y, Yoneyama K. (2008a) Sorgomol, germination stimulant for root parasitic plants, produced by Sorghum bicolor. Tetrahedron Lett 49: 2066–2068 [Google Scholar]
  121. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Yokota T, Takeuchi Y, Yoneyama K. (2008b) Isolation and identification of alectrol as (+)-orobanchyl acetate, a germination stimulant for root parasitic plants. Phytochemistry 69: 427–431 [DOI] [PubMed] [Google Scholar]
  122. Xie X, Yoneyama K, Yoneyama K. (2010) The strigolactone story. Annu Rev Phytopathol 48: 93–117 [DOI] [PubMed] [Google Scholar]
  123. Yokota T, Sakai H, Okuno K, Yoneyama K, Takeuchi Y. (1998) Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49: 1967–1973 [Google Scholar]
  124. Yoneyama K, Kisugi T, Xie X, Yoneyama K. (2013) Chemistry of strigolactones: why and how do plants produce so many strigolactones? In de Bruijn FJ, ed, Molecular Microbial Ecology of the Rhizosphere: Two Volume Set, John Wiley & Sons, Inc., Hoboken, NJ, pp 373–379 [Google Scholar]
  125. Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K. (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235: 1197–1207 [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K. (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227: 125–132 [DOI] [PubMed] [Google Scholar]
  127. Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K. (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179: 484–494 [DOI] [PubMed] [Google Scholar]
  128. Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H. (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225: 1031–1038 [DOI] [PubMed] [Google Scholar]
  129. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, et al. (2013) D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406–410 [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D. (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag Sci 65: 478–491 [DOI] [PubMed] [Google Scholar]
  131. Zwanenburg B, Nayak SK, Charnikhova TV, Bouwmeester HJ. (2013) New strigolactone mimics: structure-activity relationship and mode of action as germinating stimulants for parasitic weeds. Bioorg Med Chem Lett 23: 5182–5186 [DOI] [PubMed] [Google Scholar]

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