Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis

Yanxia Zhang; Aalt D J van Dijk; Adrian Scaffidi; Gavin R. Flematti; Manuel Hofmann; Tatsiana Charnikhova; Francel Verstappen; Jo Hepworth; Sander van der Krol; Ottoline Leyser; Steven M. Smith; Binne Zwanenburg; Salim Al-Babili; Carolien Ruyter-Spira; Harro J. Bouwmeester

doi:10.1038/nchembio.1660

Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis

Yanxia Zhang, Aalt D J van Dijk, Adrian Scaffidi, Gavin R. Flematti, Manuel Hofmann, Tatsiana Charnikhova, Francel Verstappen, Jo Hepworth, Sander van der Krol, Ottoline Leyser, Steven M. Smith, Binne Zwanenburg, Salim Al-Babili, Carolien Ruyter-Spira, Harro J. Bouwmeester

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307 Scopus citations

Abstract

Strigolactones (SLs) are a class of phytohormones and rhizosphere signaling compounds with high structural diversity. Three enzymes, carotenoid isomerase DWARF27 and carotenoid cleavage dioxygenases CCD7 and CCD8, were previously shown to convert all-trans-β-carotene to carlactone (CL), the SL precursor. However, how CL is metabolized to SLs has remained elusive. Here, by reconstituting the SL biosynthetic pathway in Nicotiana benthamiana, we show that a rice homolog of Arabidopsis More Axillary Growth 1 (MAX1), encodes a cytochrome P450 CYP711 subfamily member that acts as a CL oxidase to stereoselectively convert CL into ent-2'-epi-5-deoxystrigol (B-C lactone ring formation), the presumed precursor of rice SLs. A protein encoded by a second rice MAX1 homolog then catalyzes the conversion of ent-2'-epi-5-deoxystrigol to orobanchol. We therefore report that two members of CYP711 enzymes can catalyze two distinct steps in SL biosynthesis, identifying the first enzymes involved in B-C ring closure and a subsequent structural diversification step of SLs.

Original language	English (US)
Pages (from-to)	1028-1033
Number of pages	6
Journal	Nature Chemical Biology
Volume	10
Issue number	12
DOIs	https://doi.org/10.1038/nchembio.1660
State	Published - Oct 26 2014

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Zhang, Y., van Dijk, A. D. J., Scaffidi, A., Flematti, G. R., Hofmann, M., Charnikhova, T., Verstappen, F., Hepworth, J., van der Krol, S., Leyser, O., Smith, S. M., Zwanenburg, B., Al-Babili, S., Ruyter-Spira, C., & Bouwmeester, H. J. (2014). Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nature Chemical Biology, 10(12), 1028-1033. https://doi.org/10.1038/nchembio.1660

@article{980b7d2b209444f9b51413a7f11b94c5,

title = "Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis",

abstract = "Strigolactones (SLs) are a class of phytohormones and rhizosphere signaling compounds with high structural diversity. Three enzymes, carotenoid isomerase DWARF27 and carotenoid cleavage dioxygenases CCD7 and CCD8, were previously shown to convert all-trans-β-carotene to carlactone (CL), the SL precursor. However, how CL is metabolized to SLs has remained elusive. Here, by reconstituting the SL biosynthetic pathway in Nicotiana benthamiana, we show that a rice homolog of Arabidopsis More Axillary Growth 1 (MAX1), encodes a cytochrome P450 CYP711 subfamily member that acts as a CL oxidase to stereoselectively convert CL into ent-2'-epi-5-deoxystrigol (B-C lactone ring formation), the presumed precursor of rice SLs. A protein encoded by a second rice MAX1 homolog then catalyzes the conversion of ent-2'-epi-5-deoxystrigol to orobanchol. We therefore report that two members of CYP711 enzymes can catalyze two distinct steps in SL biosynthesis, identifying the first enzymes involved in B-C ring closure and a subsequent structural diversification step of SLs.",

author = "Yanxia Zhang and {van Dijk}, {Aalt D J} and Adrian Scaffidi and Flematti, {Gavin R.} and Manuel Hofmann and Tatsiana Charnikhova and Francel Verstappen and Jo Hepworth and {van der Krol}, Sander and Ottoline Leyser and Smith, {Steven M.} and Binne Zwanenburg and Salim Al-Babili and Carolien Ruyter-Spira and Bouwmeester, {Harro J.}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Y. Wang from the Institute of Genetics and Developmental Biology at the Chinese Academy of Science for the p35s:OsD27:PJTK13 plasmid and K. Yoneyama (Weed Science Center, Utsunomiya University, Utsunomiya, Japan) and T. Asami (Department of Applied Biological Chemistry, The University of Tokyo, Japan) for supplying SL standards. We thank J. Beekwilder and K. Cankar (Plant Research International, Wageningen, the Netherlands) for technical advice on the yeast assays and B. Ramakers (Nijmegen University) for technical support with the CD spectra measurement of CL. We thank A. Reeder from the Centre for Microscopy, Characterisation and Analysis (University of Western Australia (UWA)) and M. Clarke from the Centre for Metabolomics (UWA) for technical assistance and instrument access. We acknowledge funding by the Netherlands Organization for Scientific Research (VICI grant 865.06.002 and equipment grant 834.08.001 to H.J.B.), the Australian Research Council (LP0882775 for A.S. and FT110100304 for G.R.F.) and the UK Biotechnology and Biological Sciences Research Council (for J.H. and O.L.). Research reported in this publication was supported by the King Abdullah University of Science and Technology and was cofinanced by the Centre for BioSystems Genomics, which is part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research.",

year = "2014",

month = oct,

day = "26",

doi = "10.1038/nchembio.1660",

language = "English (US)",

volume = "10",

pages = "1028--1033",

journal = "Nature Chemical Biology",

issn = "1552-4450",

publisher = "Nature Publishing Group",

number = "12",

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Zhang, Y, van Dijk, ADJ, Scaffidi, A, Flematti, GR, Hofmann, M, Charnikhova, T, Verstappen, F, Hepworth, J, van der Krol, S, Leyser, O, Smith, SM, Zwanenburg, B, Al-Babili, S, Ruyter-Spira, C & Bouwmeester, HJ 2014, 'Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis', Nature Chemical Biology, vol. 10, no. 12, pp. 1028-1033. https://doi.org/10.1038/nchembio.1660

TY - JOUR

T1 - Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis

AU - Zhang, Yanxia

AU - van Dijk, Aalt D J

AU - Scaffidi, Adrian

AU - Flematti, Gavin R.

AU - Hofmann, Manuel

AU - Charnikhova, Tatsiana

AU - Verstappen, Francel

AU - Hepworth, Jo

AU - van der Krol, Sander

AU - Leyser, Ottoline

AU - Smith, Steven M.

AU - Zwanenburg, Binne

AU - Al-Babili, Salim

AU - Ruyter-Spira, Carolien

AU - Bouwmeester, Harro J.

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Y. Wang from the Institute of Genetics and Developmental Biology at the Chinese Academy of Science for the p35s:OsD27:PJTK13 plasmid and K. Yoneyama (Weed Science Center, Utsunomiya University, Utsunomiya, Japan) and T. Asami (Department of Applied Biological Chemistry, The University of Tokyo, Japan) for supplying SL standards. We thank J. Beekwilder and K. Cankar (Plant Research International, Wageningen, the Netherlands) for technical advice on the yeast assays and B. Ramakers (Nijmegen University) for technical support with the CD spectra measurement of CL. We thank A. Reeder from the Centre for Microscopy, Characterisation and Analysis (University of Western Australia (UWA)) and M. Clarke from the Centre for Metabolomics (UWA) for technical assistance and instrument access. We acknowledge funding by the Netherlands Organization for Scientific Research (VICI grant 865.06.002 and equipment grant 834.08.001 to H.J.B.), the Australian Research Council (LP0882775 for A.S. and FT110100304 for G.R.F.) and the UK Biotechnology and Biological Sciences Research Council (for J.H. and O.L.). Research reported in this publication was supported by the King Abdullah University of Science and Technology and was cofinanced by the Centre for BioSystems Genomics, which is part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research.

PY - 2014/10/26

Y1 - 2014/10/26

N2 - Strigolactones (SLs) are a class of phytohormones and rhizosphere signaling compounds with high structural diversity. Three enzymes, carotenoid isomerase DWARF27 and carotenoid cleavage dioxygenases CCD7 and CCD8, were previously shown to convert all-trans-β-carotene to carlactone (CL), the SL precursor. However, how CL is metabolized to SLs has remained elusive. Here, by reconstituting the SL biosynthetic pathway in Nicotiana benthamiana, we show that a rice homolog of Arabidopsis More Axillary Growth 1 (MAX1), encodes a cytochrome P450 CYP711 subfamily member that acts as a CL oxidase to stereoselectively convert CL into ent-2'-epi-5-deoxystrigol (B-C lactone ring formation), the presumed precursor of rice SLs. A protein encoded by a second rice MAX1 homolog then catalyzes the conversion of ent-2'-epi-5-deoxystrigol to orobanchol. We therefore report that two members of CYP711 enzymes can catalyze two distinct steps in SL biosynthesis, identifying the first enzymes involved in B-C ring closure and a subsequent structural diversification step of SLs.

AB - Strigolactones (SLs) are a class of phytohormones and rhizosphere signaling compounds with high structural diversity. Three enzymes, carotenoid isomerase DWARF27 and carotenoid cleavage dioxygenases CCD7 and CCD8, were previously shown to convert all-trans-β-carotene to carlactone (CL), the SL precursor. However, how CL is metabolized to SLs has remained elusive. Here, by reconstituting the SL biosynthetic pathway in Nicotiana benthamiana, we show that a rice homolog of Arabidopsis More Axillary Growth 1 (MAX1), encodes a cytochrome P450 CYP711 subfamily member that acts as a CL oxidase to stereoselectively convert CL into ent-2'-epi-5-deoxystrigol (B-C lactone ring formation), the presumed precursor of rice SLs. A protein encoded by a second rice MAX1 homolog then catalyzes the conversion of ent-2'-epi-5-deoxystrigol to orobanchol. We therefore report that two members of CYP711 enzymes can catalyze two distinct steps in SL biosynthesis, identifying the first enzymes involved in B-C ring closure and a subsequent structural diversification step of SLs.

UR - http://hdl.handle.net/10754/594213

UR - http://www.nature.com/articles/nchembio.1660

UR - http://www.scopus.com/inward/record.url?scp=84921022340&partnerID=8YFLogxK

U2 - 10.1038/nchembio.1660

DO - 10.1038/nchembio.1660

M3 - Article

C2 - 25344813

SN - 1552-4450

VL - 10

SP - 1028

EP - 1033

JO - Nature Chemical Biology

JF - Nature Chemical Biology

IS - 12

ER -

Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis

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