Carlactone is an endogenous biosynthetic precursor for strigolactones

Seto, Yoshiki; Sado, Aika; Asami, Kei; Hanada, Atsushi; Umehara, Mikihisa; Akiyama, Kazuo; Yamaguchi, Shinjiro

doi:10.1073/pnas.1314805111

Cited by 290 publications

(250 citation statements)

References 34 publications

(134 reference statements)

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“…This finding implies that the graft-transmissible mobile products in Arabidopsis could be CL-and CLA-related products. Previous reports of other strigolactones in Arabidopsis (7,8) have not been repeated (3,6).…”

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confidence: 94%

“…1). These three proteins can sequentially convert β-carotene into carlactone (CL), an intermediate molecule so far detected in root extracts from both rice and Arabidopsis (2,3). In Arabidopsis, the isomerase is encoded by DWARF27 (D27), whereas CCD7 and CCD8 are encoded by MORE AXILLARY GROWTH 3 (MAX3) and MAX4, respectively (Fig.…”

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confidence: 99%

“…A second MAX1 enzyme oxidizes 4DO to make orobanchol (4). In Arabidopsis, the situation is less clear, because it has only a single MAX1 gene, and the encoded protein oxidizes C19 of CL to produce carlactonoic acid (CLA), but it does not apparently catalyze formation of B and C rings (3,4,6) (Fig. 1).…”

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confidence: 99%

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LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis

Brewer

Yoneyama

Filardo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Strigolactones are a group of plant compounds of diverse but related chemical structures. They have similar bioactivity across a broad range of plant species, act to optimize plant growth and development, and promote soil microbe interactions. Carlactone, a common precursor to strigolactones, is produced by conserved enzymes found in a number of diverse species. Versions of the MORE AXILLARY GROWTH1 (MAX1) cytochrome P450 from rice and Arabidopsis thaliana make specific subsets of strigolactones from carlactone. However, the diversity of natural strigolactones suggests that additional enzymes are involved and remain to be discovered. Here, we use an innovative method that has revealed a missing enzyme involved in strigolactone metabolism. By using a transcriptomics approach involving a range of treatments that modify strigolactone biosynthesis gene expression coupled with reverse genetics, we identified LATERAL BRANCHING OXIDOREDUCTASE (LBO), a gene encoding an oxidoreductase-like enzyme of the 2-oxoglutarate and Fe(II)-dependent dioxygenase superfamily. Arabidopsis lbo mutants exhibited increased shoot branching, but the lbo mutation did not enhance the max mutant phenotype. Grafting indicated that LBO is required for a graft-transmissible signal that, in turn, requires a product of MAX1. Mutant lbo backgrounds showed reduced responses to carlactone, the substrate of MAX1, and methyl carlactonoate (MeCLA), a product downstream of MAX1. Furthermore, lbo mutants contained increased amounts of these compounds, and the LBO protein specifically converts MeCLA to an unidentified strigolactone-like compound. Thus, LBO function may be important in the later steps of strigolactone biosynthesis to inhibit shoot branching in Arabidopsis and other seed plants.plant | branching | strigolactone | biosynthesis | Arabidopsis

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LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis

Brewer

Yoneyama

Filardo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Among SL synthesis components, D27 encodes a β-carotene isomerase that converts all-trans-β-carotene into 9-cis-β-carotene (13,14). MAX3/RMS5/D17/DAD3 and MAX4/RMS1/D10/DAD1 encode the carotenoid cleavage dioxygenase 7 (CCD7) and CCD8, leading to the formation of carlactone, which is catalyzed further by MAX1/OsMAX1 to yield SL compounds (12,15,16). For the SL signaling components, MAX2/RMS4/D3 encodes an F-box protein participating in SL perception (17)(18)(19), D14/DAD2 encodes a protein of the α/β-fold hydrolase superfamily, a proposed SL receptor (20)(21)(22)(23)(24)(25), and D53 encodes a Clp protease family protein as a repressor (26,27).…”

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confidence: 99%

Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis

Sang

Chen

Liu

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Tiller angle, a key agronomic trait for achieving ideal plant architecture and increasing grain yield, is regulated mainly by shoot gravitropism. Strigolactones (SLs) are a group of newly identified plant hormones that are essential for shoot branching/ rice tillering and have further biological functions as yet undetermined. Through screening for suppressors of lazy1 (sols), a classic rice mutant exhibiting large tiller angle and defective shoot gravitropism, we identified multiple SOLS that are involved in the SL biosynthetic or signaling pathway. We show that SL biosynthetic or signaling mutants can rescue the spreading phenotype of lazy1 (la1) and that SLs can inhibit auxin biosynthesis and attenuate rice shoot gravitropism, mainly by decreasing the local indoleacetic acid content. Although both SLs and LA1 are negative regulators of polar auxin transport, SLs do not alter the lateral auxin transport of shoot base, unlike LA1, which is a positive regulator of lateral auxin transport in rice. Genetic evidence demonstrates that SLs and LA1 participate in regulating shoot gravitropism and tiller angle in distinct genetic pathways. In addition, the SL-mediated shoot gravitropism is conserved in Arabidopsis. Our results disclose a new role of SLs and shed light on a previously unidentified mechanism underlying shoot gravitropism. Our study indicates that SLs could be considered as an important tool to achieve ideal plant architecture in the future. P lant shoot gravitropism is a process in which plants perceive gravity stimuli and reorient the direction of growth during the plant growth and development. Gravitropism is a dynamic process, including the perception of gravity, transduction of the corresponding information into a biochemical signal, transmission of the biochemical signal to a response site, and organ curvature (1). Genetic studies have disclosed that shoot endodermal cells act as statocytes for shoot gravitropism (2). Amyloplast sedimentation transduces the gravitropic signal and leads to auxin redistribution, resulting in a higher auxin level on the lower side than on the upper side (1, 3). Although auxin redistribution upon gravistimulation plays an important role in shoot gravitropism, the mechanism by which auxin regulates shoot gravitropism is not yet understood.In rice the tiller angle, which is defined as the angle between the tiller and main culm, plays a key role in determining rice plant architecture and thus grain yield (4). Several genes controlling the tiller angle have been identified previously in rice, including LAZY1 (LA1), TILLER ANGLE CONTROL1 (TAC1), PROSTRATE GROWTH1 (PROG1), and LOOSE PLANT ARCHITECTURE1 (LPA1) (5-9). Among these genes, LA1 and LPA1 are reported to regulate tiller angle through shoot gravitropism. In the la1 mutant, the polar auxin transport (PAT) is enhanced, and the lateral auxin transport is decreased, resulting in a disturbance of auxin asymmetric distribution in the shoot base and therefore the tiller-spreading phenotype of rice plants (5).Strigolactones (S...

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“…Considering that the E. coli strains used mainly accumulate all-trans-configured carotenoids, these results indicated that SLs are synthesized via the intermediate b-apo-13-carotenone produced by CCD7 and CCD8 from all-trans-b-carotene. However, a recent in vitro study suggested a new path to SLs via carlactone [24], a SLs-like compound that has been very recently also identified in planta [41]. This pathway starts with the D27-catalyzed isomerization of all-trans-into 9-cis-b-carotene that is cleaved by CCD7 to yield b-ionone and 9-cis-b-apo-10 0 -carotenal used by CCD8 to form carlactone, supposedly by catalyzing a combination of different reactions [24].…”

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On the substrate‐ and stereospecificity of the plant carotenoid cleavage dioxygenase 7

et al. 2014

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a b s t r a c tStrigolactones are phytohormones synthesized from carotenoids via a stereospecific pathway involving the carotenoid cleavage dioxygenases 7 (CCD7) and 8. CCD7 cleaves 9-cis-b-carotene to form a supposedly 9-cis-configured b-apo-10 0 -carotenal. CCD8 converts this intermediate through a combination of yet undetermined reactions into the strigolactone-like compound carlactone. Here, we investigated the substrate and stereo-specificity of the Arabidopsis and pea CCD7 and determined the stereo-configuration of the b-apo-10 0 -carotenal intermediate by using Nuclear Magnetic Resonance Spectroscopy. Our data unequivocally demonstrate the 9-cis-configuration of the intermediate. Both CCD7s cleave different 9-cis-carotenoids, yielding hydroxylated 9-cis-apo-10 0 -carotenals that may lead to hydroxylated carlactones, but show highest affinity for 9-cis-b-carotene.

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Carlactone is an endogenous biosynthetic precursor for strigolactones

Cited by 290 publications

References 34 publications

LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis

LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis

Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis

On the substrate‐ and stereospecificity of the plant carotenoid cleavage dioxygenase 7

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