Plant Physiology Preview. Published on July 18, 2014, as DOI:10.1104/pp.114.244939
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Strigolactone involvement in root development, response to abiotic stress and
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interactions with the biotic soil environment
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Yoram Kapulnik and Hinanit Koltai
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Institute of Plant Sciences, ARO, Volcani Center
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Corresponding Author: Yoram Kapulnik, [email protected]; Tel.: +972-50-6220461; Fax:
+972-3-9604180
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Running title: Strigolactone affect root development and response
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One Sentence Summary: Strigolactones, new plant hormones, play a role in root
development, root response to nutrient deficiency and plant interactions in the rhizosphere.
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ABSTRACT
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Strigolactones, recently discovered as plant hormones, regulate the development of different
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plant parts. In the root, they regulate root architecture and affect root-hair length and density.
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Their biosynthesis and exudation increase under low phosphate levels and they are associated
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with root responses to these conditions. Their signaling pathway in the plant includes protein
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interactions and ubiquitin-dependent repressor degradation. In the root, they lead to changes in
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actin architecture and dynamics, and in localization of the PIN auxin transporter in the plasma
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membrane. Strigolactones are also involved with communication in the rhizosphere. They are
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necessary for germination of parasitic plant seeds, they enhance hyphal branching of arbuscular
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mycorrhizal fungi and they promote rhizobial symbiosis. The current review focuses on the role
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played by strigolactones in root development, their response to nutrient deficiency and their
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involvement with plant interactions in the rhizosphere.
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INTRODUCTION
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Strigolactones have been recently discovered as plant hormones (Gomez-Roldan et al.,
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2008; Umehara et al., 2008) that are produced by a wide variety of plant species (Xie et al.,
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2010; Yoneyama et al., 2013). Several different types of strigolactones can be produced by a
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single plant species, and different varieties of the same plant species may produce mixtures of
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different types and quantities of strigolactone molecules (Xie et al., 2010; Yoneyama et al.,
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2013). Strigolactones are also produced in primitive plants, including Embryophyta and Charales
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(Delaux et al., 2012). In all cases, they are produced and exuded in small amounts (e.g., Sato et
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al., 2003; Yoneyama et al., 2007a; 2007b). Strigolactones are produced primarily in roots, but
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their biosynthesis is not limited to the root system and also occurs in other plant parts (reviewed
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by Koltai and Beveridge, 2013).
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Although strigolactone biosynthesis derives from the carotenoid-synthesis pathway (Booker
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et al., 2004; Matusova et al., 2005), only some of the proteins that are crucial for biosynthesis
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have been identified to date. In the tested higher plant species, three plastid-localized proteins
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have been found to be involved in the first stages of strigolactone biosynthesis (Booker et al.,
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2004, Matusova et al., 2005). One is a carotenoid isomerase, DWARF27 (D27), characterized in
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rice (Oryza sativa L.), Arabidopsis (Arabidopsis thaliana) and pea (Pisum sativum) (Lin et al.,
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2009, Waters et al., 2012a; Adler et al., 2012). It can convert all-trans-β-carotene into 9’-cis-β-
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carotene (Alder et al., 2012). The latter is then oxidatively tailored, cleaved and cyclized by two
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double-bond-specific cleavage enzymes, carotenoid cleavage dioxygenase (CCD) 7 and 8
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(Booker et al., 2004; Schwartz et al., 2004), resulting in the bioactive strigolactone precursor
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carlactone (Alder et al., 2012). The conversion of carlactone to strigolactone has not been
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characterized, but may include MAX1, a class-III cytochrome P450 monooxygenase (Booker et
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al., 2005; Alder et al., 2012; Cardoso et al., 2014). The presence of CCD enzymes has been
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demonstrated in several diverse higher plants (Delaux et al., 2012). Moss (Physcomitrella
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patens) also contains homologs of these three genes and accordingly, can produce strigolactones
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(Proust et al., 2011). However, only some of these genes are present in other basal plants and
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algae (Delaux et al., 2012). Approximately 15 strigolactones have been structurally characterized
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to date (Ruyter-Spira et al., 2013); all consist of an ABC-ring system connected via an enol ether
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bridge to a butenolide D ring (Xie et al., 2010).
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As plant hormones, strigolactones regulate the development of different plant parts. The
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first indication that strigolactones function as plant hormones came from an examination of
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hyperbranching mutants. These mutants' phenotype could not be attributed to altered levels of, or
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response to one of the established plant hormones known at the time. Hence, a novel signal that
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was associated with this phenotype was suggested (Beveridge et al., 1997). Later, this signal was
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identified to be strigolactones, and to act as a long-distance branching factor that suppresses
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growth of preformed axillary buds (Gomez-Roldan et al., 2008; Umehara et al., 2008).
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Strigolactones dampen auxin transport in the main stem, thereby enhancing competition
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between axillary branches and restraining axillary bud outgrowth (e.g., Bennett et al., 2006;
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Mouchel and Leyser, 2007; Ongaro and Leyser, 2008; Crawford et al., 2010; Domagalska and
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Leyser, 2011). Accordingly, strigolactones were demonstrated to act by increasing the rate of
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removal of PIN1, the auxin export protein, from the plasma membrane of xylem parenchyma
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cells in the stem. This activity was demonstrated by both computational model and experimental
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data, and was correlated to the level of shoot branching observed in various mutant combinations
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and strigolactone treatments (Shinohara et al., 2013). In pea, strigolactones were shown to induce
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the expression of the bud-specific target gene BRANCHED1 (BRC1), which encodes a
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transcription factor repressing bud outgrowth (Dun et al., 2012), and to be an auxin-promoted
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secondary messenger (Dun et al., 2012; 2013; Brewer et al., 2009; Ferguson and Beveridge,
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2009). Other activities of strigolactone include repression of adventitious-root formation
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(Rasmussen et al., 2012) and plant height (de Saint Germain et al., 2013). They also induce
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secondary growth in the stem (Agusti et al., 2011). Auxin positively regulates strigolactone
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biosynthesis by elevating the expression of both MAX3 and MAX4. It has been suggested that
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auxin and strigolactone modulate each other's levels and distribution, forming a dynamic
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feedback loop between the two hormones (Hayward et al., 2009).
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As noted, although the main site of strigolactone synthesis is the roots, part of their activity
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is in the shoot. Therefore, strigolactones are expected be transported upward in the plant, from
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root to shoot. Evidence to support this suggestion comes from Kohlen et al., (2011), who showed
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the presence of the strigolactone orobanchol in the xylem sap of Arabidopsis. Another means of
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strigolactone transport is probably via specific transporters. The Petunia hybrida ABC
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transporter PDR1, localized mainly in the bud/leaf vasculature and subepidermal cells of the
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root, was identified as a cellular strigolactone exporter. It was shown to regulate the level of
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symbiosis of arbuscular mycorrhizal fungi (AMF) (discussed further on) and axillary-shoot
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branching (Kretzschmar et al., 2012).
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Strigolactones also act in the root to determine root architecture. However, even before
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strigolactones were identified as plant hormones, they were known to be involved with
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communication in the rhizosphere. The current review focuses on strigolactone activity in the
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roots as regulators of root-system architecture, root-hair length and primary root meristem, and
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on aspects of their signaling. Their involvement with the root response to nutrient growth
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conditions will also be presented and discussed. Moreover, the effects of strigolactone on root–
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rhizosphere communication will be presented, along with some implications on the evolution of
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these interactions and their implementation.
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STRIGOLACTONES REGULATE ROOT DEVELOPMENT
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One of the first pieces of evidence suggesting that strigolactones have a role in the
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development of root-system architecture was the finding that Arabidopsis mutants in the
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strigolactone response or biosynthesis have more lateral roots than the wild type (WT; Kapulnik
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et al., 2011a; Ruyter-Spira et al., 2011). Accordingly, treatment of seedlings with GR24 (a
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synthetic and biologically active strigolactone; Johnson et al., 1976; Umehara et al., 2008;
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Gomez-Roldan et al., 2008) repressed lateral root formation in the WT and strigolactone-
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synthesis mutants (max3 and max4), but not in the strigolactone-response mutant (max2),
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suggesting that the negative effect of strigolactones on lateral root formation is MAX2-
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dependent (Kapulnik et al., 2011a; Ruyter-Spira et al., 2011). This negative effect on lateral root
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formation was reversed in Arabidopsis under phosphate deficiency (Ruyter-Spira et al., 2011;
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discussed further on).
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Strigolactones are also suggested to regulate primary root length. GR24 led to elongation of
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the primary root and to an increase in meristem cell number in a MAX2-dependent manner
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(Ruyter-Spira et al., 2011; Koren et al., 2013). Accordingly, under conditions of carbohydrate
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limitation, a shorter primary root and less primary meristem cells were detected in strigolactone-
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deficient and response mutants in comparison to the WT (Ruyter-Spira et al., 2011).
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Furthermore, in rice, a major quantitative trait locus on chromosome 1—qSLB1.1—was
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identified for the exudation of strigolactones, tillering, and induction of Striga germination
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(Cardoso et al., 2014). Several root-architectural traits were mapped in the same region (Topp et
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al., 2013), suggesting that this locus may be involved in both strigolactone synthesis and root-
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system architecture.
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Notably, expression of MAX2 under the SCARECROW (SCR) promoter was sufficient to
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confer a response to GR24 in a max2-1 mutant background for both lateral root formation and
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cell number in the primary root meristem (Koren et al., 2013). Since SCR is expressed mainly in
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the root endodermis and quiescence center (Sabatini et al., 2003), these results point to an
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important role for the endodermis in strigolactone regulation of root architecture.
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Another one of strigolactones' effects in roots is on root-hair length. Exogenous
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supplementation of various synthetic strigolactone analogs induced root-hair elongation in
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Arabidopsis, in both the WT and strigolactone-deficient mutants (max3 and max4), but not in the
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strigolactone-response mutant max2, suggesting that the effect of strigolactones on root-hair
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elongation is mediated via MAX2 (Kapulnik et al., 2011a; Cohen et al., 2013). Furthermore,
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response to auxin and ethylene signaling is required, at least in part, for the positive effect of
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strigolactone on root-hair elongation. However, MAX2-dependent strigolactone signaling is not
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necessary for the root-hair elongation induced by auxin (Kapulnik et al., 2011b). Hence,
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strigolactones affect root-hair length at least in part through the auxin and ethylene pathways
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(Koltai, 2011). Here too, expression of SCR::MAX2 was sufficient to confer root-hair elongation
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in roots in response to GR24 (Koren et al., 2013). Since root-hair elongation is regulated in the
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epidermis, the sufficiency of MAX2 expression under SCR (expressed mainly in the root
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endodermis and quiescence center) for GR24 sensitivity suggests that strigolactones act non-cell-
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autonomously at short-range.
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To summarize, strigolactones play a regulatory role in root development. At least part of this
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activity is performed non-cell-autonomously, and may involve modulation of auxin transport, as
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discussed further on.
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STRIGOLACTONE SIGNALING PATHWAY
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As indicated earlier for shoots, in the root, evidence also indicates a role for strigolactones in
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the regulation of PIN protein activity. One piece of evidence comes from studies of tomato roots,
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in which exogenous supplementation of 2,4-D (a synthetic auxin that is not secreted by auxin6
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efflux carriers) led to reversion of the GR24-related root effect, suggesting functional
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involvement of GR24 with auxin export (Koltai et al. 2010). Another piece of evidence comes
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from studies in Arabidopsis, where treatment of seedlings with GR24 led to a decrease in PIN-
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FORMED (PIN1)–GFP intensity in lateral root primordia, suggesting that GR24 regulates PIN1
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and modulates auxin flux in roots, and as a result, alters the auxin optima necessary for lateral
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root formation (Ruyter-Spira et al., 2011). Furthermore, in Arabidopsis, following GR24
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treatment that leads to root-hair elongation, PIN2 polarization was changed in the plasma
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membrane of the root epidermis in the WT but not in the max2 mutant. In addition, in a MAX2-
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dependent manner, GR24 treatment led to increased PIN2 endocytosis, increased endosomal
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movement in the epidermal cells, and changes in actin filament architecture and dynamics
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(Pandya-Kumar et al., 2014). Together, these results suggest that strigolactones affect plasma
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membrane localization of PIN proteins. At least for PIN2 in the root, they probably do so by
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regulating the architecture and dynamics of actin filaments and PIN endocytosis, which are
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important for PIN2 polarization (Pandya-Kumar et al., 2014; Figure 1).
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Upstream of those events are probably those associated with strigolactone reception. One
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of the components of strigolactone reception was identified several years ago as an F-box
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protein, MAX2/D3/RMS4 (Stirnberg et al., 2002; Ishikawa et al., 2005; Johnson et al., 2006). An
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additional component of strigolactone signaling is D14, which is a protein of the α/β-fold
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hydrolase superfamily (Arite et al., 2009). Petunia DAD2, a homolog of D14, was shown to
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interact in a yeast two-hybrid assay with petunia MAX2A only in the presence of GR24,
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resulting in hydrolysis of GR24 by DAD2 (Hamiaux et al., 2012). In addition, in rice, D14 was
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shown to bind to GR24 (Kagiyama et al., 2013) and to cleave strigolactones (Nakamura et al.,
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2013).
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Moreover, via a Skp, Cullin, F-box (SCF)-containing complex (Moon et al., 2004), and in a
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D14- and D3-dependent manner, it was shown in rice that strigolactones induce degradation of
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D53, a class I Clp ATPase protein. D53 acts as a repressor of axillary bud outgrowth, and its
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degradation by strigolactones prevents its activity in promoting axillary bud outgrowth (Jiang et
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al., 2013; Zhou et al., 2013; Figure 1). Furthermore, in Arabidopsis, strigolactones were
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suggested to induce, in a MAX2-dependent manner, proteasome-mediated degradation of D14
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(Chevalier et al., 2014), suggesting a negative regulatory circuit of strigolactones and their own
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signaling.
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This regulatory module of strigolactone/D14-like/D3-like/SCF is likely to have been
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conserved in plant evolution (Waldie et al., 2014). As indicated above, it was shown to be
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associated with strigolactone-regulated shoot development (Jiang et al., 2013; Zhou et al., 2013).
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However it is not clear whether this or a similar reception system acts in the roots. It might be
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that diversity in this module confers tissue specificity. Different D14-like proteins attached to
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D3/MAX2 may confer different substrate specificity and as a result, a specific effect on plant
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development. For example, a KAI2 (D14-LIKE)–MAX2-dependent pathway is responsible for
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regulating seed germination, seedling growth and leaf and rosette development in response to
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karrikins—strigolactone-analogous compounds originally found in forest-fire smoke (Flematti et
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al., 2004; Waters et al., 2012b; Nelson et al., 2011; Waters et al., 2014). Modules for
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strigolactone response that are composed of other α/β-fold hydrolases and/or degradation of
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other repressors could potentially lead to execution of the strigolactone-related processes in roots
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(Figure 1).
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STRIGOLACTONES ARE INVOLVED IN ROOT RESPONSES TO ABIOTIC STRESS
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CONDITIONS
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Strigolactones seem to have been involved in plant responses to environmental stimuli
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from their early evolution. In the moss P. patens, they determine the patterns of growth and
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responses between neighboring colonies (Proust et al., 2011). In higher plants, they are involved
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in both shoot and root architecture in response to nutritional conditions.
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Pi is the inorganic form of phosphorus (P) that is available to plants. It is an essential
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macronutrient for growth and development and in many places, it is considered to be a limiting
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factor for growth (Bieleski, 1973; Maathuis, 2009). To cope with Pi deprivation, plants modify
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their growth pattern and architecture. The shoot-to-root ratio is reduced under these conditions
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(e.g., Ericsson, 1995); shoot branching is inhibited (reviewed by Domagalska and Leyser, 2011),
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and root architecture is altered (Osmont et al., 2007; López-Bucio et al., 2003). Elongation of the
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primary root is inhibited under conditions of Pi deficiency (Sánchez-Calderón et al., 2005) and
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lateral root development is promoted (Nacry et al., 2005), probably for increased foraging of
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subsurface soil. Following extended deprivation, root growth is also inhibited (Nacry et al.,
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2005). It should be noted, however, that these general patterns are not identical in all plant
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species. For example, under Pi deprivation, primary root growth is inhibited in some Arabidopsis
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ecotypes but not in others (Chevalier et al., 2003).
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Several plant hormones are known to regulate root-system architecture in response to
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nutrient conditions. For example, under low Pi conditions, the changes in lateral root formation
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in Arabidopsis have been suggested to result from increased auxin sensitivity, mediated by an
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increase in the expression of the auxin receptor TIR1 (Pérez-Torres et al., 2008). Strigolactones
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might be another plant hormone involved in the regulation of root-system architecture in
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response to nutrient conditions. Although under conditions of sufficient Pi, strigolactones
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negatively regulate lateral root formation (Kapulnik et al., 2011a), they reverse their effect to
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positive regulation when Pi is limited (Ruyter-Spira et al., 2011). This suggests that
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strigolactones act as another key regulator of lateral root formation, promoting their development
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under low Pi conditions and repressing their emergence once Pi is abundant.
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The length and density of root hairs are increased under Pi-deficient conditions, probably
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to expand root surface area and enhance nutrient acquisition (Bates and Lynch, 2000; Péret et al.,
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2011; Gilroy and Jones, 2000). Indeed, the plant’s ability to absorb nutrients from the soil is
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suggested to be directly associated with root-hair length and number (Sanchez-Calderon et al.,
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2005; reviewed by Gilroy and Jones, 2000). The recorded ability of strigolactone analogs to
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increase root-hair length (Kapulnik et al., 2011a) may indicate their role in root-hair elongation
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as an adaptive process in plants to growth conditions.
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Also of significance is the dependence on strigolactones for the seedling response to Pi
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deprivation, in terms of increasing root-hair density. Arabidopsis mutants, defective in
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strigolactone biosynthesis or response, have a reduced ability to increase their root-hair density
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in response to low Pi shortly after germination (Mayzlish-Gati et al., 2012). In accordance with
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the suggestion that low Pi response is mediated by an increase in TIR1 expression (Pérez-Torres
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et al., 2008), the strigolactone-response mutant, under conditions of Pi deprivation, displayed a
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reduction, rather than induction of TIR1 expression (Mayzlish-Gati et al., 2012).
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The reduced ability of strigolactone mutants to respond to low Pi conditions shortly after
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germination may compromise survival of these seedlings under these conditions (Mayzlish-Gati
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et al., 2012). These findings suggest an important role for strigolactones in plant adaptation to
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stress. However, later on in plant development, even the strigolactone mutants recover, and are
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able to respond to low Pi conditions (Mayzlish-Gati et al., 2012). This seedling recovery
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suggests the involvement of other mechanisms that are not dependent on strigolactones for
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responding to Pi deprivation, which are effective later on in plant development.
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Similarly, strigolactone involvement in responses to phosphate and nitrate was shown in
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rice, by analyzing the response of strigolactone-synthesis (d10 and d27) or insensitive (d3)
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mutants to reduced concentrations of Pi or nitrate (NO3−). Reduced Pi or NO3− concentrations
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led to increased seminal root length and decreased lateral root density in the WT, but not in the
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strigolactone mutants. Application of GR24 restored seminal root length and lateral root density
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in the WT and in the strigolactone-biosynthesis mutants, but not in the strigolactone-response
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mutant, suggesting that strigolactones are involved with the response to Pi and NO3− in rice as
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well, leading to a D3-dependent change in rice root growth. In addition, based on changes in the
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transport of radiolabeled indole-3-acetic acid, it was suggested that the mechanisms underlying
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this regulatory role of D3/strigolactones involves modulation of auxin transport from shoots to
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roots (Sun et al., 2014).
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Pi deprivation leads to an increase in strigolactone exudation. Nitrogen (N) deficiency has
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also been shown to increase strigolactone exudation. Nevertheless, it might be that N deficiency
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affects strigolactone levels via its effect on P levels in the shoot. Indeed, a correlation was found
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between shoot Pi levels and strigolactone exudation across plant species (Yoneyama et al.,
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2007a; 2007b; 2012). A clear correlation was also found in both Arabidopsis and rice between
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this elevation in strigolactone levels and a decrease in shoot branching under restricted-Pi growth
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conditions. In Arabidopsis, in correlation with the changes in shoot architecture, the level of the
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strigolactone orobanchol in the xylem sap was increased under Pi deficiency (Kohlen et al.,
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2011). In rice, under these conditions, tiller bud outgrowth was inhibited and root strigolactone
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(2′-epi-5-deoxystrigol) levels increased (Umehara et al., 2008). The increase in strigolactone
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biosynthesis and exudation under low Pi conditions may also induce increased branching of
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mycorrhizal hyphae (Akiyama et al., 2005; Besserer et al., 2006; 2008; Gomez-Roldan et al.,
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2008; Yoneyama et al., 2008), as detailed in the following chapters, and hence increased
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mycorrhization.
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STRIGOLACTONES ARE SIGNALS FOR PLANT INTERACTIONS
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Strigolactones were initially identified as germination stimulants of the parasitic plants
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Striga and Orobanche (e.g., Cook et al., 1972; Yokota et al., 1998; Matusova et al., 2005; Xie et
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al., 2007; 2008a; 2008b; 2009; Goldwasser et al., 2008; Gomez-Roldan et al., 2008). It was only
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later that strigolactones were also identified as stimulants of hyphal branching in AMF (e.g.,
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Akiyama et al., 2005; Besserer et al., 2006; 2008; Gomez-Roldan et al., 2008; Yoneyama et al.,
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2008). In addition, strigolactones were shown to stimulate nodulation in the legume–rhizobium
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interaction process (Foo and Davies, 2011).
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Mycorrhizal Symbiosis
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The most prevalent symbiosis on earth is the arbuscular mycorrhizal (AM) symbiosis, which
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consists of an association between the roots of higher plants and soil AMF. The AMF are
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members of the fungal phylum Glomeromycota (Redecker and Raab, 2006), and symbiotic
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associations are formed with most terrestrial vascular flowering plants (Smith and Read, 2008),
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in most cases contributing to plant development, especially under suboptimal growth conditions.
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During the symbiosis, AMF hyphae, which extend through the soil, provide a greater root
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surface area to exploit a larger volume of soil, thereby enhancing the amount of nutrients
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absorbed from the soil for the plant (Rausch and Bucher, 2002). In return, the fungus receives
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fixed carbon in the form of glucose (reviewed by Douds et al., 2000), hexoses (Shachar-Hill et
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al., 1995; Solaimand and Saito, 1997) or sucrose from the host.
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In general, the AM symbiosis is comprised of two distinct functional stages: the
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"presymbiotic stage" and the "symbiotic stage". A very detailed description of the presymbiotic
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stage confirmed that fungal spore germination in the soil and the growth of fungal hyphae are
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both stimulated in the presence of a host root (Mosse and Hepper, 1975; Gianinazzi-Pearson et
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al., 1989; Giovannetti et al., 1996; Buée et al., 2000; Nagahashi and Douds, 2000; Requena et al.,
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2007). These two phenomena, together with the hyphal branching response, may reflect unique
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communication in the rhizosphere to enhance successful mycorrhization on the host (Koske and
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Gemma, 1992).
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Purified strigolactones from root exudates or synthetic strigolactones have been shown
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capable of inducing hyphal branching in many AMF (Akiyama et al., 2005). These molecules are
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present at sub-nanogram levels in the rhizosphere (Akiyama and Hayashi, 2006; Akiyama et al.,
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2005). Similarly, the synthetic strigolactone GR24 was shown to effectively induce AMF hyphal
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branching at a concentration of 10-8 M (Gomez-Roldan et al., 2008). Accordingly, strigolactone-
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deficient mutants of pea and tomato exhibit reduced levels of AMF hyphal branching in their
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rhizosphere as compared to the response obtained in the presence of WT root exudates (Gomez-
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Roldan et al., 2008; Koltai et al., 2010b).
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In a more in-depth study, it was demonstrated that strigolactones rapidly induce changes in
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AMF energy metabolism before any gene-expression process in the fungus can be detected.
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When AMF hyphae were exposed to the synthetic strigolactone GR24, a rapid alteration (within
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60 min) in mitochondrial shape, density and motility was observed. In Gigaspora rosea hyphae,
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NADH concentrations, dehydrogenase activity and ATP content were altered within minutes by
324
application of GR24 (Besserer et al., 2006; 2008).
325
The importance of strigolactones to AMF establishment was reinforced by the observation
326
of a lower colonization rate of a tomato strigolactone-biosynthesis mutant by AMF spores than
327
that obtained in WT roots. Interestingly, these differences were less pronounced when plants
328
were inoculated with "whole inoculum" (consisting of spores, hyphae and infected roots) (Koltai
329
et al., 2010b).
330
Nevertheless, it was shown that root exudates of mycorrhitic plants induce Striga and
331
Orobanche seed germination to a lesser extent than the induction obtained by exudates of non-
332
mycorrhitic plants (Lendzemo et al., 2009; Fernández-Aparicio et al., 2010). Moreover,
333
strigolactone production was shown to be significantly reduced in roots of mycorrhitic tomato
334
plants (López-Ráez et al., 2011). Therefore, strigolactones may be negatively regulated by AMF
335
via a feedback loop. Alternatively, it may be that AMF colonization has a significant impact on
336
enhancement of AM symbiosis and consequently, increased Pi acquisition, which may then be
337
reflected in elevated levels of P content, the latter inducing suppression of strigolactone
338
biosynthesis.
339
It is not yet clear whether strigolactones have any role during fungal morphogenesis in the
340
host cortical cells or during symbiosis stages. Moreover, it is not clear whether strigolactones are
341
essential for the AMF interaction.
342
343
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344
Parasitic Plants
345
Witchweed (Striga spp.) and broomrape (Orobanche and Phelipanche spp.) are important
346
parasitic weeds that have a devastating effect on the production of many crop species, resulting
347
in economic damage and food losses worldwide (Parker, 2009). The damage conferred on crop
348
development and productivity has been summarized elsewhere (Joel, 2000; Gressel and Joel,
349
2013).
350
The communication between parasites and their host plants depends on strigolactones, as
351
signal molecules which are exuded from the host roots into the rhizosphere. These signals mostly
352
involve induction of seed germination of the parasitic plants which, within a few days, must
353
attach to their host to acquire nutrients, or die (Joel and Bar, 2013). This communication allows
354
germination of the parasitic plant at the right distance from the root surface, at the right time in
355
the season and with the right nutritional, temperature and moisture levels in the host rhizosphere.
356
Following the parasitic plant's germination, a tubercle develops underground and shoot
357
outgrowth is initiated. The shoots emerge aboveground, flower, and produce tens of thousands of
358
seeds (for a more in-depth review, the reader is referred to Joel, 2013).
359
Three types of isoprenoid compounds stimulate the germination of root-parasitic plants:
360
dihydrosorgoleone, the sesquiterpene lactones, and strigolactones (Bouwmeester et al., 2003).
361
Strigolactones are active at extremely low concentrations (on the order of 10-7 to 10-15 M; Joel,
362
2000). A variety of natural strigolactones were shown able to induce germination of Orobanche
363
minor from 10 pM strigolactones (for orobanchol, 2'-epiorobanchol and sorgomol) to 10 nM for
364
7-oxoorobanchol. The synthetic analog GR24 is 100-fold less active than natural strigolactones
365
(Kim et al., 2010). Advances in chromatography and mass spectrometry are enabling the
366
discovery and characterization of novel strigolactones.
367
368
Symbiotic Interactions with Rhizobium
369
The nitrogen-fixing bacteria of the genus Rhizobium play a fundamental role in nodule
370
formation and beneficial symbiotic interactions on the roots of legumes such as pea, bean
371
(Phaseolus vulgaris), clover (Trifolium spp.) and alfalfa (Medicago sativa). The symbiotic
372
interaction involves signal exchange between the partners that leads to mutual recognition and
373
development of the nodule structure. In short, at the preinfection stage, the bacteria sense
374
flavonoids that are secreted from the legume host roots. These flavonoid molecules, which are
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375
specific to each legume–rhizobium interaction, activate the production and secretion of
376
lipochitooligosaccharide nodulation (Nod) factors from the bacteria that are recognized by the
377
host plant. In most cases, Nod-factor perception leads to induction of a cascade of signaling
378
events, such as root-hair deformation and infection-thread formation, and is involved in triggering
379
cell division in the cortex of the root, leading to nodule organ formation. Production of Nod
380
factors and exopolysaccharides by many of the rhizobium bacteria elicits an infection thread
381
where the penetrated bacteria multiply. Intracellular bacterial cells then differentiate to
382
"bacteroids"—the nitrogen-fixing stage of the symbiosis. In addition to the morphological and
383
cellular modifications, plants and bacteria produce and respond to large groups of peptides,
384
transcriptional factors, and early and late nodulation (nod) genes. However, the molecular
385
mechanisms by which many of them are involved in the differentiation process are poorly
386
understood. Within the nodule meristem and after cell differentiation, rhizobia bacteroids supply
387
ammonia or amino acids to the plant and in return, receive organic acids as a carbon and energy
388
source (Markmann and Parniske, 2009).
389
The ability of strigolactones to alter plant-meristem development led to the search for
390
strigolactone involvement in this symbiotic interaction. The potential of strigolactones to control
391
nodulation was verified using the strigolactone-deficient rms1 mutant in pea (Pisum sativum L.)
392
(Foo and Davis, 2011). This work showed that endogenous strigolactones are positive regulators
393
of nodulation in this plant. Using rms1 mutant root exudates and root tissue that were almost
394
completely deficient in strigolactones, Foo and Davies, (2011) demonstrated a 40% reduction in
395
the number of nodules relative to WT plants that contained strigolactones. Application of GR24
396
to rms1 plants resulted in an increase in the number of nodules on the mutant roots to the level
397
obtained on the WT (without exogenous application of strigolactones). GR24 application can also
398
enhance nodule number in WT pea, M. sativa and Lotus japonicus (Soto et al., 2010; Foo and
399
Davies, 2011; Liu et al., 2013). It was also shown that strigolactones in the root, but not shoot-
400
derived factors, can regulate nodule number (Foo et al., 2014). Genetic studies indicated that
401
strigolactones may act relatively early in nodule formation, rather than during nodule
402
organogenesis (Foo et al., 2013 a, b). Moreover, it was shown that strigolactones do not influence
403
nodulation by acting directly on the rhizobium bacteria (Soto et al., 2010) or on the Ca2+
404
signaling that follows flavonoid perception (Moscatiello et al., 2010). It was suggested that
405
strigolactones are not essential for the development of a functional nodule but may be important
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406
in determining the optimal nodule number, thereby having a quantitative effect on nodulation in
407
pea (Foo et al., 2014).
408
The mechanism governing strigolactone enhancement of the nodulation process is still an
409
enigma. One potential explanation might be that strigolactones interact with auxin distribution
410
during the cell-division process that leads to nodule development. Auxin was found to be
411
accumulated in dividing cortical cells in L. japonicus and NODULE INCEPTION, a key
412
transcription factor in nodule development, was found to positively regulate this accumulation
413
(Suzaki et al., 2012). Thus, the fact that strigolactones also regulate auxin transport suggests an
414
additional regulatory path for this symbiotic interaction. Furthermore, it was shown that auxin
415
positively regulates strigolactone production (Hayward et al., 2009), which suggests a positive-
416
feedback regulation loop between auxin and strigolactones in the promotion of nodulation in
417
legume roots.
418
419
CONCLUDING REMARKS
420
421
Strigolactones are an important group of molecules. They likely developed in plants as key
422
regulators of plants' developmental adaptations to environmental conditions. Their production
423
and exudation from roots was utilized by other organisms to the benefit (AMF and rhizobia) or
424
detriment (parasitic plants) of the host plants. Strigolactones may be involved in additional cases
425
of communication in the rhizosphere, as well as in additional responses of the plant to growth
426
conditions. This is due to the high complexity of the rhizosphere (Jones and Hinsinger, 2008),
427
which is composed of (1) a multiplicity of organisms and (2) microconditions in soil “pockets”,
428
e.g., low levels of nutrients. This complexity may hinder the evaluation of additional functions of
429
strigolactones under the non-homogeneous rhizospheric conditions that are normally found in
430
nature.
431
Another interesting aspect of strigolactones is their potential use in agriculture. A number of
432
publications have discussed their implementation as inducer of suicidal seed germination of
433
parasitic plant (e.g., Zwanenburg et al., 2009; Vurro and Yoneyama, 2012; Zwanenburg et al.,
434
2013). However, strigolactones may be used in additional approaches for the development of
435
new agricultural methodologies and technologies, compatible with emerging concepts of
436
sustainable agriculture. For example, strigolactones may be used for improvement of root-system
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437
architecture, e.g., to develop a hyperbranched root system for increased nutrient-use efficiency,
438
or deeper roots for increased water-use efficiency. They may also be used for regulation of shoot
439
branching when, for example, the emergence of axillary branches is undesirable. Strigolactone
440
analogs and mimics that are specific for one activity (e.g., shoot branching) are already being
441
developed (Fukui et al., 2011; 2013; Boyer et al., 2013). Strigolactone inhibitors may be used to
442
enhance rooting of plant cuttings (Rasmussen et al., 2012), potentially promoting the propagation
443
of woody plants for the industry and for conservation of endangered species. Today's new
444
strigolactone analogs and mimics, which are under development or being synthesized
445
(Zwanenburg et al., 2009; Prandi et al., 2011), are likely to substantially promote the ability to
446
use strigolactones to the benefit of agriculture.
447
448
LITERATURE CITED
449
Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA,
450
Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-
451
dependent stimulation of secondary growth in plants. Proc Natl Acad Sci U S A 108:
452
20242-20247
453
454
455
456
Akiyama K, Hayashi H (2006) Strigolactones: Chemical Signals for Fungal Symbionts and
Parasitic Weeds in Plant Roots. Ann Bot 97: 925-931
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in
arbuscular mycorrhizal fungi. Nature 435: 824-827
457
Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester
458
H, Beyer P, Al-Babili S (2012) The path from β-Carotene to Carlactone, a strigolactone-
459
like plant hormone. Science 335: 1348-1351
460
Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009)
461
d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers.
462
Plant Cell Physiol 50: 1416-1424
463
464
465
Bates TR, Lynch JP (2000) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in
phosphorus acquisition. Am J Bot 87: 964-970
Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis
466
MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16: 553-
467
563
16
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
468
Besserer A, Becard G, Jauneau A, Roux C, Sejalon-Delmas N (2008) GR24, a synthetic
469
analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal
470
fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148: 402-413
471
Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC,
472
Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular
473
mycorrhizal fungi by activating mitochondria. PLoS Biol 4: e226
474
Beveridge CA, Symons GM, Murfet IC, Ross JJ, Rameau C (1997) The rms1 mutant of pea
475
has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but
476
increased branching controlled by graft-transmissible signal (s). Plant Physiol 115: 1251-
477
1258
478
479
Bieleski R (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev
Plant Physiol 24: 225–252
480
Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a
481
carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling
482
molecule. Curr Biol 14: 1232-1238
483
Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C,
484
Srinivasan M, Goddard P, Leyser O (2005) MAX1 Encodes a Cytochrome P450 family
485
member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-
486
inhibiting hormone. Dev Cell 8: 443-449
487
Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite
488
signalling in host–parasitic plant interactions. Curr Opin Plant Biol 6: 358-364Boyer FD,
489
de Saint germain A, Pouvreau JB, Clavé G, Pillot JP, Roux A, Rasmussen A,
490
Depuydt S, Depuydt S, Lauressergues D, dit Frey NF, Heugebaert TSA, Stevens CV,
491
Geelen D, Goormachtig S, Rameau C (2014) New strigolactone analogues as plant
492
hormones with low activities in the rhizosphere. Mol Plant: 7: 675-690
493
Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts
494
downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol
495
150: 482-493
496
Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of
497
Arbuscular Mycorrhizal Fungi is induced by a branching factor partially purified from
498
plant root exudates. Mol Plant Microbe Interact 13: 693-698
17
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
499
Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO, Meharg C,
500
Wright MH, Liu J, Meng X, Wang Y, Li J, McCouch SR, Leyser O, Price AH,
501
Bouwmeester HJ, Ruyter-Spira C (2014) Natural variation of rice strigolactone
502
biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci
503
U S A: 6: 2379-2384
504
Chevalier F, Nieminen K, Sánchez-Ferrero JC, Rodríguez ML, Chagoyen M, Hardtke CS,
505
Cubas P (2014) Strigolactone promotes degradation of DWARF14, an α/β Hydrolase
506
essential for strigolactone signaling in Arabidopsis. Plant Cell : 26:1134-1150
507
Chevalier F, Pata M, Nacry P, Doumas P, Rossignol M (2003) Effects of phosphate
508
availability on the root system architecture: large‐scale analysis of the natural variation
509
between Arabidopsis accessions. Plant Cell Environ 26: 1839-1850
510
Cohen M, Prandi C, Occhiato EG, Tabasso S, Wininger S, Resnick N, Steinberger Y,
511
Koltai H, Kapulnik Y (2013) Structure-function relations of strigolactone analogs:
512
Activity as plant hormones and plant interactions. Molecular Plant 6: 141-152
513
Cook CE, Whichard LP, Wall M, Egley GH, Coggon P, Luhan PA, McPhail AT (1972)
514
Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for
515
witchweed (Striga lutea). Journal of the American Chemical Society 94: 6198-6199
516
Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Muller D,
517
Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot
518
branches by dampening auxin transport. Development 137: 2905-2913
519
de Saint Germain A, Ligerot Y, Dun EA, Pillot J-P, Ross JJ, Beveridge CA, Rameau C
520
(2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant
521
Physiol 163: 1012-1025
522
Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF,
523
Yoneyama K, Bécard G, Séjalon-Delmas N (2012) Origin of strigolactones in the green
524
lineage. New Phytol 195: 857-871
525
526
527
528
Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat
Rev Mol Cell Biol 12: 211-221
Douds Jr DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism
of arbuscular mycorrhizas. In Y Kapulnik , DD Douds Jr, eds, Arbuscular
18
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
529
mycorrhizas: physiology and function, Kluwer Academic Publishers,Dordrecht, The
530
Netherlands, pp 107–130.
531
532
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
533
Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2013) Dynamics of strigolactone
534
function and shoot branching responses in Pisum sativum. Molecular Plant 6: 128-140
535
Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. In
536
LO Nilsson, RF Hüttl, UT Johansson, eds, Nutrient Uptake and Cycling in Forest
537
Ecosystems, Vol 62. Springer Netherlands, pp 205-214
538
539
Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating
shoot branching. Plant Physiol 149: 1929-1944
540
Fernández-Aparicio M, GarcÍA-Garrido JM, Ocampo JA, Rubiales D (2010) Colonisation
541
of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche
542
species seed germination. Weed Res 50: 262-268
543
544
Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that
promotes seed germination. Science 305: 977-977
545
Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234: 1073-1081
546
Foo E, Ferguson B, Reid J (2014) The potential roles of strigolactones and brassinosteroids in
547
548
549
550
the autoregulation of nodulation pathway. Ann Bot: PMID: 24694828
Foo E, Yoneyama K, Hugill C, Quittenden LJ, Reid JB (2013a) Strigolactones: internal and
external signals in plant symbioses. Plant Signal Behav 8: e23168
Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013b) Strigolactones and the
551
regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:
552
76-87
553
554
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
555
Fukui K, Ito S, Ueno K, Yamaguchi S, Kyozuka J, Asami T (2011) New branching inhibitors
556
and their potential as strigolactone mimics in rice. Bioorg Med Chem Lett 21: 4905-4908
557
Gianinazzi-Pearson V, Gianinazzi S (1989) Cellular and genetical aspects of interactions
558
between hosts and fungal symbionts in mycorrhizae. Genome 31: 336-341
19
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
559
560
561
Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient
uptake. Trends Plant Sci 5: 56-60
Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in fungal
562
recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New
563
Phytol 133: 65-71
564
Goldwasser Y, Yoneyama K, Xie X, Yoneyama K (2008) Production of Strigolactones by
565
Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant
566
Growth Regul 55: 21-28
567
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F,
568
Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA,
569
Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature
570
455: 189-194
571
572
573
Gressel J, Joel DM (2013) Weedy Orobanchaceae: The Problem. In DM Joel, J Gressel,
LJ Musselman, eds, Parasitic Orobanchaceae, Springer, Berlin, pp 309-312
Hamiaux C, Drummond RSM, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD,
574
Snowden KC (2012) DAD2 Is an α/β Hydrolase likely to be involved in the perception
575
of the plant branching hormone, strigolactone. Curr Biol 22: 2032-2036
576
577
Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and
strigolactone in shoot branching control. Plant Physiol 151: 400-412
578
Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of
579
tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46: 79-86
580
Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y (2013)
581
DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401-405
582
583
Joel DM (2000) The long-term approach to parasitic weeds control: manipulation of specific
developmental mechanisms of the parasite. Crop Prot 19: 753-758
584
Joel DM (2013) The Haustorium and the Life Cycles of Parasitic Orobanchaceae. In DM Joel, J
585
Gressel, LJ Musselman, eds, Parasitic Orobanchaceae, Springer, Berlin, pp 21-23
586
587
588
589
Joel DM, Bar H (2013) The Seed and the Seedling. In DM Joel, J Gressel, LJ Musselman, eds,
Parasitic Orobanchaceae, Springer, Berlin pp 147-165
Johnson AW, Rosebery G, Parker C (1976) A novel approach to Striga and Orobanche control
using synthetic germination stimulants. Weed Research 16: 223-227
20
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
590
Johnson X, Brcich T, Dun EA, Goussot M, Haurogne K, Beveridge CA, Rameau C (2006)
591
Branching genes are conserved across species. Genes controlling a novel signal in Pea are
592
coregulated by other long-distance signals. Plant Physiol 142: 1014-1026
593
Jones D, Hinsinger P (2008) The rhizosphere: complex by design. Plant Soil 312: 1-6
594
Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, Yamaguchi S, Hakoshima T
595
(2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways.
596
Genes Cells 18: 147-160
597
Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C,
598
Séjalon-Delmas N, Combier J-P, Bécard G, Belausov E, Beeckman T, Dor E,
599
Hershenhorn J, Koltai H (2011a) Strigolactones affect lateral root formation and root-
600
hair elongation in Arabidopsis. Planta 233: 209-216
601
Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H
602
(2011b) Strigolactones interact with ethylene and auxin in regulating root-hair elongation
603
in Arabidopsis. J Exp Bot 62: 2915-2924
604
Kim HI, Xie X, Kim HS, Chun JC, Yoneyama K, Nomura T, Takeuchi Y, Yoneyama K
605
(2010) Structure-activity relationship of naturally occurring strigolactones in Orobanche
606
minor seed germination stimulation. J Pestic Sci: 35:344-347
607
Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F,
608
Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported
609
through the xylem and play a key role in shoot architectural response to phosphate
610
deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155: 974-987
611
Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190: 545-549
612
Koltai H, Beveridge CA (2013) Strigolactones and the coordinated development of shoot and
613
root. In F Baluška, eds, Long-Distance Systemic Signaling and Communication in Plants,
614
Springer, Berlin, pp 189-204
615
Koltai H, Dor E, Hershenhorn J, Joel D, Weininger S, Lekalla S, Shealtiel H, Bhattacharya
616
C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010a) Strigolactones’ effect on root
617
growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant
618
Growth Regul 29: 129-136
619
620
Koltai H, LekKala SP, Bhattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E,
Yoneyama K, Yoneyama K, Hershenhorn J, Joel DM, Kapulnik Y (2010b) A tomato
21
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
621
strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions.
622
J Exp Bot 61: 1739-1749
623
Koren D, Resnick N, Mayzlish-Gati E,, Belausov E, Weininger S, Kapulnik Y, Koltai H
624
(2013) Strigolactone signaling in the endodermis is sufficient to restore root responses
625
and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol 198: 866-874
626
Koske RE, Gemma JN (1992) Fungal reactions to plants prior to mycorrhizal formation. In MF
627
Allen, eds, Mycorrhizal functioning: an integrative plant-fungal process. Chapman &
628
Hall, New York, pp 3-36
629
Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D,
630
Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls
631
strigolactone-dependent symbiotic signalling and branching. Nature 483: 341-344
632
Lendzemo V, Kuyper T, Vierheilig H (2009) Striga seed-germination activity of root exudates
633
and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced
634
due to root colonization by arbuscular mycorrhizal fungi. Mycorrhiza 19: 287-294
635
Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009)
636
DWARF27, an iron-containing protein required for the biosynthesis of strigolactones,
637
regulates rice tiller bud outgrowth. Plant Cell 21: 1512-1525
638
Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P,
639
Lovisolo C, Bouwmeester HJ, Cardinale F (2013) CAROTENOID CLEAVAGE
640
DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate
641
nodulation in the model legume Lotus japonicus. J Exp Bot 64: 1967-1981
642
643
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
644
López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011) Arbuscular
645
mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:
646
294-297
647
648
649
650
Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol
12: 250-258
Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: How novel
are nodules? Trends Plant Sci 14: 77-86
22
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
651
Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ
652
(2005) The strigolactone germination stimulants of the plant-parasitic Striga and
653
Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139: 920-934
654
Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB,
655
Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y Wininger S, Resnick N, Cohen M,
656
Kapulnik Y, Koltai H (2012) Strigolactones are involved in root response to low
657
phosphate conditions in Arabidopsis. Plant Physiol 160: 1329-1341
658
659
660
661
662
663
664
665
666
Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development.
Plant Cell 16: 3181-3195
Moscatiello R, Squartini A, Mariani P, Navazio L (2010) Flavonoid‐induced calcium
signalling in Rhizobium leguminosarum bv. viciae. New Phytol 188: 814-823
Mosse B, Hepper C (1975) Vesicular-arbuscular mycorrhizal infections in root organ cultures.
Physiological Plant Pathology 5: 215-223
Mouchel CF, Leyser O (2007) Novel phytohormones involved in long-range signaling. Curr
Opin Plant Biol 10: 473-476
Nacry P, Canivenc Gv, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005)
667
A role for auxin redistribution in the responses of the root system architecture to
668
phosphate starvation in Arabidopsis. Plant Physiol 138: 2061-2074
669
Nagahashi G, Douds Jr DD (2000) Partial separation of root exudate components and their
670
effects upon the growth of germinated spores of AM fungi. Mycological Research 104:
671
1453-1464
672
Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X, Ito E, Ito S, Park
673
SH, Miyauchi Y, Asano A, Totsuka N, Ueda T, Tanokura M, Asami T (2013)
674
Molecular mechanism of strigolactone perception by DWARF14. Nature Comm 4: 2613
675
Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA,
676
Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and
677
strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci U S A 108: 8897-
678
8902
679
Ongaro V, Leyser O (2008) Hormonal control of shoot branching. J Exp Bot 59: 67-74
680
Osmont KS, Sibout R, Hardtke CS (2007) Hidden Branches: Developments in Root System
681
Architecture. Annu Rev Plant Biol 58: 93-113
23
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
682
Pandya‐Kumar N, Shema R, Kumar M, Mayzlish‐Gati E, Levy D, Zemach H, Belausov E,
683
Wininger S, Abu‐Abied M, Kapulnik Y, Koltai H (2014) Strigolactone analog GR24
684
triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New
685
Phytol 202: 1469-8137
686
687
Parker C (2009) Observations on the current status of Orobanche and Striga problems
worldwide. Pest Manag Sci 65: 453-459
688
Péret B, Clement M, Nussaume L, Desnos T (2011) Root developmental adaptation to
689
phosphate starvation: better safe than sorry. Trends Plant Sci 16: 442-450
690
Pérez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S,
691
Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root
692
development in Arabidopsis by modulating auxin sensitivity via a mechanism involving
693
the TIR1 auxin receptor. Plant Cell 20: 3258-3272
694
Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Miletto I
695
(2011) New potent fluorescent analogues of strigolactones: synthesis and biological
696
activity in parasitic weed germination and fungal branching. European Journal of Organic
697
Chemistry 2011: 3781-3793
698
Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F,
699
Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum
700
sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539
701
Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb
702
T, Goormachtig S, Beeckman T (2012) Strigolactones suppress adventitious rooting in
703
Arabidopsis and pea. Plant Physiol 158: 1976-1987
704
705
706
707
708
Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta
216: 23-37
Redecker D, Raab P (2006) Phylogeny of the Glomeromycota (arbuscular mycorrhizal fungi):
recent developments and new gene markers. Mycologia 98: 885-895
Requena N, Serrano E, Ocón A, Breuninger M (2007) Plant signals and fungal perception
709
during arbuscular mycorrhiza establishment. Phytochemistry 68: 33-40
710
Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of
711
strigolactones. Trends Plant Sci 18: 72-83
24
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
712
Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N,
713
Cardoso C, Lopez-Raez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H
714
(2011) Physiological effects of the synthetic strigolactone analog GR24 on root system
715
architecture in Arabidopsis: Another belowground role for strigolactones? Plant Physiol
716
155: 721-734
717
718
719
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
Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F,
720
Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate
721
developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46: 174-
722
184
723
Sato D, Awad AA, Chae SH, Yokota T, Sugimoto Y, Takeuchi Y, Yoneyama K (2003)
724
Analysis of strigolactones, germination stimulants for Striga and Orobanche, by high-
725
performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 51:
726
1162-1168
727
Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid
728
cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound
729
inhibits lateral branching. J Biol Chem 279: 46940-46945
730
Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995)
731
Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek.
732
Plant Physiol 108: 7-15
733
Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching
734
by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma
735
membrane. PLoS biology 11: e1001474
736
Smith S, Read D, eds (2008) Mycorrhizal Symbiosis (3rd edn). Academic Press
737
Solaimanand MZ, Saito M (1997) Use of sugars by intraradical hyphae of arbuscular
738
mycorrhizal fungi revealed by radiorespirometry. New Phytol 136: 533-538
739
Soto MJ, Fernandez-Aparicio Mn, Castellanos-Morales V, Garcia-Garrido JM, Ocampo
740
JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of
741
strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:
742
383-385
25
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
743
744
745
Stirnberg P, van de Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral
branching in Arabidopsis. Development 129: 1131-1141
Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014)
746
Strigolactones are involved in phosphate-and nitrate-deficiency-induced root
747
development and auxin transport in rice. J Exp Bot: PMID 24596173
748
Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and
749
negative regulation of cortical cell division during root nodule development in Lotus
750
japonicus is accompanied by auxin response. Development 139: 3997-4006
751
Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee C-R, Zurek PR, Symonova O, Zheng Y,
752
Bucksch A, Mileyko Y, Galkovskyi T (2013) 3D phenotyping and quantitative trait
753
locus mapping identify core regions of the rice genome controlling root architecture. Proc
754
Natl Acad Sci U S A 110: E1695-E1704
755
Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H,
756
Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of
757
shoot branching by new terpenoid plant hormones. Nature 455: 195-200
758
Vurro M, Yoneyama K (2012) Strigolactones—intriguing biologically active compounds:
759
perspectives for deciphering their biological role and for proposing practical application.
760
Pest Manag Sci 68: 664-668
761
762
763
Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development:
lessons from shoot branching. Plant J: PMID:24620182
Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012a) The Arabidopsis
764
ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development
765
by strigolactones. Plant Physiol 159: 1073-1085
766
Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012b)
767
Specialisation within the DWARF14 protein family confers distinct responses to
768
karrikins and strigolactones in Arabidopsis. Development 139: 1285-1295
769
Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM (2014) The karrikin response
770
771
system of Arabidopsis. The Plant Journal: PMID:24433542
Xie X, Kusumoto D, Takeuchi Y, Yoneyama K, Yamada Y, Yoneyama K (2007) 2′-Epi-
772
orobanchol and Solanacol, Two Unique Strigolactones, Germination Stimulants for Root
773
Parasitic Weeds, Produced by Tobacco. J Agric Food Chem 55: 8067-8072
26
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
774
Xie X, Yoneyama K, Harada Y, Fusegi N, Yamada Y, Ito S, Yokota T, Takeuchi Y,
775
Yoneyama K (2009) Fabacyl acetate, a germination stimulant for root parasitic plants
776
from Pisum sativum. Phytochemistry 70: 211-215
777
Xie X, Yoneyama K, Kusumoto D, Yamada Y, Takeuchi Y, Sugimoto Y, Yoneyama K
778
(2008a) Sorgomol, germination stimulant for root parasitic plants, produced by Sorghum
779
bicolor. Tetrahedron Letters 49: 2066-2068
780
Xie X, Yoneyama K, Kusumoto D, Yamada Y, Yokota T, Takeuchi Y, Yoneyama K
781
(2008b) Isolation and identification of alectrol as (+)-orobanchyl acetate, a germination
782
stimulant for root parasitic plants. Phytochemistry 69: 427-431
783
784
785
Xie X, Yoneyama K, Yoneyama K (2010) The Strigolactone Story. Annu Rev Phytopathol 48:
93-117
Yokota T, Sakai H, Okuno K, Yoneyama K, Takeuchi Y (1998) Alectrol and orobanchol,
786
germination stimulants for Orobanche minor, from its host red clover. Phytochemistry
787
49: 1967-1973
788
Yoneyama K, Kisugi T, Xie X, Yoneyama K (2013) Chemistry of Strigolactones: Why and
789
How do Plants Produce so Many Strigolactones?, In FJ de Bruijn ed Molecular Microbial
790
Ecology of the Rhizosphere: Two volume set, John Wiley & Sons, Inc., NJ, pp:373-379
791
Yoneyama K, Xie X, Kim H, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K
792
(2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and
793
exudation? Planta 235: 1197-1207
794
Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K
795
(2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the
796
production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular
797
mycorrhizal fungi and root parasites. Planta 227: 125-132
798
Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H,
799
Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and
800
arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179: 484-494
801
Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red
802
clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and
803
germination stimulant for root parasites. Planta 225: 1031-1038
27
Downloaded from on June 17, 2017 - Published by www.plantphysiol.org
Copyright © 2014 American Society of Plant Biologists. All rights reserved.
804
Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L (2013)
805
D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature
806
504: 406-410
807
Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D (2009)
808
Structure and function of natural and synthetic signalling molecules in parasitic weed
809
germination. Pest Manag Sci 65: 478-491
810
Zwanenburg B, Nayak SK, Charnikhova TV, Bouwmeester HJ (2013) New strigolactone
811
mimics: Structure–activity relationship and mode of action as germinating stimulants for
812
parasitic weeds. Bioorg Med Chem Lett 23: 5182-5186
813
814
815
816
817
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Figure legend
819
820
Figure 1. A model of the putative signaling pathway of strigolactone in roots. An α/β-fold
821
hydrolase protein may serve as the strigolactone receptor. It may interact with MAX2 and as a
822
result, lead to degradation by ubiquitination of a repressor (reviewed by Waldie et al., 2014).
823
These or similar events may lead to changes in the architecture and dynamics of actin filaments
824
and PIN endocytosis which is important for PIN2 polarization. As a result, PIN2 protein
825
polarization is affected, which may lead to changes in auxin flux, and to execution of
826
strigolactone-associated root effects, such as root-hair elongation.
827
828
28
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Copyright © 2014 American Society of Plant Biologists. All rights reserved.
MAX2
SCF
complex
α/β
HYDROLASE
REPRESSOR
?
Key
Strigolactones
Ubiquitin
PIN containing membrane
Root responses
Actin filament
(e.g., root hair elongation)
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