Shoot branching is a major determinant of plant architecture and is highly regulated by endogenous and environmental cues. Two classes of hormones, auxin and cytokinin, have long been known to have an important involvement in controlling shoot branching. Previous studies using a series of mutants with enhanced shoot branching suggested the existence of a third class of hormone(s) that is derived from carotenoids, but its chemical identity has been unknown. Here we show that levels of strigolactones, a group of terpenoid lactones, are significantly reduced in some of the branching mutants. Furthermore, application of strigolactones inhibits shoot branching in these mutants. Strigolactones were previously found in root exudates acting as communication chemicals with parasitic weeds and symbiotic arbuscular mycorrhizal fungi. Thus, we propose that strigolactones act as a new hormone class-or their biosynthetic precursors-in regulating above-ground plant architecture, and also have a function in underground communication with other neighbouring organisms.
Strigolactones (SLs) were originally isolated from plant root exudates as germination stimulants for root parasitic plants of the family Orobanchaceae, including witchweeds (Striga spp.), broomrapes (Orobanche and Phelipanche spp.), and Alectra spp., and so were regarded as detrimental to the producing plants. Their role as indispensable chemical signals for root colonization by symbiotic arbuscular mycorrhizal fungi was subsequently unveiled, and SLs then became recognized as beneficial plant metabolites. In addition to these functions in the rhizosphere, it has been recently shown that SLs or their metabolites are a novel class of plant hormones that inhibit shoot branching. Furthermore, SLs are suggested to have other biological functions in rhizosphere communications and in plant growth and development.
Strigolactones (SLs) stimulate seed germination of root parasitic plants and induce hyphal branching of arbuscular mycorrhizal fungi in the rhizosphere. In addition, they have been classified as a new group of plant hormones essential for shoot branching inhibition. It has been demonstrated thus far that SLs are derived from carotenoid via a biosynthetic precursor carlactone (CL), which is produced by sequential reactions of DWARF27 (D27) enzyme and two carotenoid cleavage dioxygenases CCD7 and CCD8. We previously found an extreme accumulation of CL in the more axillary growth1 (max1) mutant of Arabidopsis, which exhibits increased lateral inflorescences due to SL deficiency, indicating that CL is a probable substrate for MAX1 (CYP711A1), a cytochrome P450 monooxygenase. To elucidate the enzymatic function of MAX1 in SL biosynthesis, we incubated CL with a recombinant MAX1 protein expressed in yeast microsomes. MAX1 catalyzed consecutive oxidations at C-19 of CL to convert the C-19 methyl group into carboxylic acid, 9-desmethyl-9-carboxy-CL [designated as carlactonoic acid (CLA)]. We also identified endogenous CLA and its methyl ester [methyl carlactonoate (MeCLA)] in Arabidopsis plants using LC-MS/MS. Although an exogenous application of either CLA or MeCLA suppressed the growth of lateral inflorescences of the max1 mutant, MeCLA, but not CLA, interacted with Arabidopsis thaliana DWARF14 (AtD14) protein, a putative SL receptor, as shown by differential scanning fluorimetry and hydrolysis activity tests. These results indicate that not only known SLs but also MeCLA are biologically active in inhibiting shoot branching in Arabidopsis.strigolactone | biosynthesis | cytochrome P450 | Arabidopsis | rice S trigolactones (SLs) are allelochemicals, exuded from plant roots, that stimulate seed germination of root parasitic plants, Striga spp., Orobanche spp., and Phelipanche spp. (1). The hyphal branching of the biotrophic arbuscular mycorrhizal (AM) fungi is also induced by SLs in the vicinity of host roots to ensure symbiosis with host plants (2). SLs are not only host recognition signals in the rhizosphere but also play important roles in the SLproducing plants themselves. Since the mid-1990s, the existence of novel hormone-like signals involved in shoot branching inhibition of plants had been proposed following the isolation and analysis of mutants with increased shoot branching, ramosus (rms) of pea (Pisum sativum), decreased apical dominance (dad) of petunia (Petunia hybrida), more axillary growth (max) of Arabidopsis (Arabidopsis thaliana), and dwarf (d) and high tillering dwarf (htd) of rice (Oryza sativa) (3-6). Recently, these mutants have been identified as SL-deficient or -insensitive mutants, providing decisive evidence that SLs function as shoot branchinhibiting hormones (7,8). In addition, further characterization of these mutants has shown that SLs affect root growth and development, leaf shape and senescence, internode elongation, secondary growth, and drought and salinity stress responses (9-11).Despit...
Strigolactones (SLs) or their derivatives have recently been defined as novel phytohormones that regulate root development. However, it remains unclear whether SLs mediate root growth in response to phosphorus (P) and nitrogen (N) deficiency. In this study, the responses of root development in rice (Oryza sativa L.) to different levels of phosphate and nitrate supply were investigated using wild type (WT) and mutants defective in SL synthesis (d10 and d27) or insensitive to SL (d3). Reduced concentration of either phosphate or nitrate led to increased seminal root length and decreased lateral root density in WT. Limitation of either P or N stimulated SL production and enhanced expression of D10, D17, and D27 and suppressed expression of D3 and D14 in WT roots. Mutation of D10, D27, or D3 caused loss of sensitivity of root response to P and N deficiency. Application of the SL analogue GR24 restored seminal root length and lateral root density in WT and d10 and d27 mutants but not in the d3 mutant, suggesting that SLs were induced by nutrient-limiting conditions and led to changes in rice root growth via D3. Moreover, P or N deficiency or GR24 application reduced the transport of radiolabelled indole-3-acetic acid and the activity of DR5::GUS auxin reporter in WT and d10 and d27 mutants. These findings highlight the role of SLs in regulating rice root development under phosphate and nitrate limitation. The mechanisms underlying this regulatory role involve D3 and modulation of auxin transport from shoots to roots.
Summary• The aims of this study were to investigate the appearance of strigolactones in the green lineage and to determine the primitive function of these molecules.• We measured the strigolactone content of several isolated liverworts, mosses, charophyte and chlorophyte green algae using a sensitive biological assay and LC-MS ⁄ MS analyses. In parallel, sequence comparison of strigolactone-related genes and phylogenetic analyses were performed using available genomic data and newly sequenced expressed sequence tags. The primitive function of strigolactones was determined by exogenous application of the synthetic strigolactone analog, GR24, and by mutant phenotyping.• Liverworts, the most basal Embryophytes and Charales, one of the closest green algal relatives to Embryophytes, produce strigolactones, whereas several other species of green algae do not. We showed that GR24 stimulates rhizoid elongation of Charales, liverworts and mosses, and rescues the phenotype of the strigolactone-deficient Ppccd8 mutant of Physcomitrella patens.• These findings demonstrate that the first function of strigolactones was not to promote arbuscular mycorrhizal symbiosis. Rather, they suggest that the strigolactones appeared earlier in the streptophyte lineage to control rhizoid elongation. They may have been conserved in basal Embryophytes for this role and then recruited for the stimulation of colonization by glomeromycotan fungi.
Plant derived sesquiterpene strigolactones, which have previously been characterized as germination stimulants for root parasitic plants, have recently been identified as the branching factors which induce hyphal branching morphogenesis, a critical step in host recognition by arbuscular mycorrhizal (AM) fungi. We show here that, in red clover plants (Trifolium pratense L.), which is known as a host for both AM fungi and the root holoparasitic plant Orobanche minor Sm., reduced supply of phosphorus (P) but not of other elements examined (N, K, Mg, Ca) in the culture medium significantly promotes the release of a strigolactone, orobanchol, by the roots of this plant. In red clover plants, the level of orobanchol exudation appeared to be regulated by P availability and was in good agreement with germination stimulation activity of the root exudates. This implies that under P deficiency, plant roots attract not only symbiotic fungi but also root parasitic plants through the release of strigolactones. This is the first report demonstrating that nutrient availability influences both symbiotic and parasitic interactions in the rhizosphere.
Strigolactones released from plant roots induce hyphal branching of symbiotic arbuscular mycorrhizal (AM) fungi and germination of root parasitic weeds, Striga and Orobanche spp. We already demonstrated that, in red clover plants (Trifolium pratense L.), a host for both AM fungi and the root holoparasitic plant Orobanche minor Sm., reduced supply of phosphorus (P) but not of other elements examined (N, K, Ca, Mg) in the culture medium significantly promoted the secretion of a strigolactone, orobanchol, by the roots of this plant. Here we show that in the case of sorghum [Sorghum bicolor (L.) Moench], a host of both the root hemiparasitic plant Striga hermonthica and AM fungi, N deficiency as well as P deficiency markedly enhanced the secretion of a strigolactone, 5-deoxystrigol. The 5-deoxystrigol content in sorghum root tissues also increased under both N deficiency and P deficiency, comparable to the increase in the root exudates. These results suggest that strigolactones may be rapidly released after their production in the roots. Unlike the situation in the roots, neither N nor P deficiency affected the low content of 5-deoxystrigol in sorghum shoot tissues.
SUMMARYStrigolactones are a novel class of plant hormones controlling shoot branching in seed plants. They also signal host root proximity during symbiotic and parasitic interactions. To gain a better understanding of the origin of strigolactone functions, we characterised a moss mutant strongly affected in strigolactone biosynthesis following deletion of the CAROTENOID CLEAVAGE DIOXYGENASE 8 (CCD8) gene. Here, we show that wild-type Physcomitrella patens produces and releases strigolactones into the medium where they control branching of protonemal filaments and colony extension. We further show that Ppccd8 mutant colonies fail to sense the proximity of neighbouring colonies, which in wild-type plants causes the arrest of colony extension. The mutant phenotype is rescued when grown in the proximity of wild-type colonies, by exogenous supply of synthetic strigolactones or by ectopic expression of seed plant CCD8. Thus, our data demonstrate for the first time that Bryophytes (P. patens) produce strigolactones that act as signalling factors controlling developmental and potentially ecophysiological processes. We propose that in P. patens, strigolactones are reminiscent of quorum-sensing molecules used by bacteria to communicate with one another.
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