Strigolactone involvement in root development, response to abiotic stress and interactions with the

29 Pages·2014·0.61 MB·English

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.: [phone]; Fax:
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[phone]
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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
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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- -carotene into 9’-cis- -
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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 auxin-
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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 / -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 / -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 (NO −). Reduced Pi or NO − 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 NO − 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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