Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs

Catarina Cardoso; Yanxia Zhang; Muhammad Jamil; Jo Hepworth; Tatsiana Charnikhova; Stanley O. N. Dimkpa; Caroline Meharg; Mark H. Wright; Junwei Liu; Xiangbing Meng; Yonghong Wang; Jiayang Li; Susan R. McCouch; Ottoline Leyser; Adam H. Price; Harro J. Bouwmeester; Carolien Ruyter-Spira

doi:10.1073/pnas.1317360111

Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs

Catarina Cardoso, Yanxia Zhang, Muhammad Jamil, Jo Hepworth, Tatsiana Charnikhova, Stanley O. N. Dimkpa, Caroline Meharg, Mark H. Wright, Junwei Liu, Xiangbing Meng, Yonghong Wang, Jiayang Li, Susan R. McCouch, Ottoline Leyser, Adam H. Price, Harro J. Bouwmeester^*, Carolien Ruyter-Spira

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

115 Citations (Scopus)

Abstract

Rice (Oryza sativa) cultivar Azucena-belonging to the Japonica subspecies-exudes high strigolactone (SL) levels and induces high germination of the root parasitic plant Striga hermonthica. Consistent with the fact that SLs also inhibit shoot branching, Azucena is a low-tillering variety. In contrast, Bala, an Indica cultivar, is a low-SL producer, stimulates less Striga germination, and is highly tillered. Using a Bala x Azucena F6 population, a major quantitative trait loci-qSLB1.1- for the exudation of SL, tillering, and induction of Striga germination was detected on chromosome 1. Sequence analysis of the corresponding locus revealed a rearrangement of a 51- to 59-kbp stretch between 28.9 and 29 Mbp in the Bala genome, resulting in the deletion of two cytochrome P450 genes-SLB1 and SLB2-with high homology to the Arabidopsis SL biosynthesis gene, MAX1. Both rice genes rescue the Arabidopsis max1-1 highly branched mutant phenotype and increase the production of the SL, ent-2'-epi-5-deoxystrigol, when overexpressed in Bala. Furthermore, analysis of this region in 367 cultivars of the publicly available Rice Diversity Panel population shows that the rearrangement at this locus is a recurrent natural trait associated with the Indica/Japonica divide in rice.

Original language	English
Pages (from-to)	2379-2384
Number of pages	6
Journal	PNAS
Volume	111
Issue number	6
DOIs	https://doi.org/10.1073/pnas.1317360111
Publication status	Published - 11 Feb 2014

Bibliographical note

Acknowledgments
We thank Koichi Yoneyama (Utsunomiya University, Japan), Yukihiro Sugimoto (Kobe University, Japan), and Tadao Asami (University of Tokyo, Japan) for the kind provision of ent-2′-epi-orobanchol, orobanchol, 5-deoxystrigol, 2′-epi-5-deoxystrigol, and [2H]6-2′-epi-5-deoxystrigol; and Binne Zwanenburg (University of Nijmegen, The Netherlands) for providing GR24. A.H.P. and H.J.B. thank Pieter Ouwerkerk for bringing them together. This work was supported by the Higher Education Commission Pakistan (to M.J.); Netherlands Organization for Scientific Research Vici Grant 865.06.002 (to H.J.B.) and Equipment Grant 834.08.001 (to H.J.B.); the Centre for BioSystems Genomics, part of the Netherlands Genomics Initiative/Netherlands Organisation for Scientific Research (to H.J.B.); National Science Foundation Plant Genome Research Grant 1026555 (to S.R.M.); US Department of Agriculture National Institute for Food and Agriculture Grant 2009-65300-05661 (to S.R.M.); United Kingdom Biotechnology and Biological Science Research Council (to J.H.); Government of the Rivers State of Nigeria Postgraduate Scholarship (to S.O.N.D.); and National Natural Science Foundation of China Grant 31161130535 (to Y.W.). Bala sequencing was supported by European Union FP6 Project 015468 (“CEDROME”) and a Monitoring Agricultural Resources grant; Azucena sequencing was supported by Biotechnology and Biological Sciences Research Council–Department for International Development Grant BBF0041841.

Keywords

QTL
plant hormone
CYP450
Arbuscular mycorrhizal fungi
Quantitative Trait Loci
Tiller Bud Outgrowth
Striga-Hermonthica
Oryza-Sativa
Phosphate deficiency
Root morphology
Arabidopsis
Architecture
INHIBITION

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Adam Price
- Biological Sciences, Aberdeen Centre For Environmental Sustainability - Personal Chair
Person: Academic

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Cardoso, C., Zhang, Y., Jamil, M., Hepworth, J., Charnikhova, T., Dimkpa, S. O. N., Meharg, C., Wright, M. H., Liu, J., Meng, X., Wang, Y., Li, J., McCouch, S. R., Leyser, O., Price, A. H., Bouwmeester, H. J., & Ruyter-Spira, C. (2014). Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. PNAS, 111(6), 2379-2384. https://doi.org/10.1073/pnas.1317360111

Cardoso, C, Zhang, Y, Jamil, M, Hepworth, J, Charnikhova, T, Dimkpa, SON, Meharg, C, Wright, MH, Liu, J, Meng, X, Wang, Y, Li, J, McCouch, SR, Leyser, O, Price, AH, Bouwmeester, HJ & Ruyter-Spira, C 2014, 'Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs', PNAS, vol. 111, no. 6, pp. 2379-2384. https://doi.org/10.1073/pnas.1317360111

@article{c15734094b784fa7b02ff465cf4aadca,

title = "Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs",

abstract = "Rice (Oryza sativa) cultivar Azucena-belonging to the Japonica subspecies-exudes high strigolactone (SL) levels and induces high germination of the root parasitic plant Striga hermonthica. Consistent with the fact that SLs also inhibit shoot branching, Azucena is a low-tillering variety. In contrast, Bala, an Indica cultivar, is a low-SL producer, stimulates less Striga germination, and is highly tillered. Using a Bala x Azucena F6 population, a major quantitative trait loci-qSLB1.1- for the exudation of SL, tillering, and induction of Striga germination was detected on chromosome 1. Sequence analysis of the corresponding locus revealed a rearrangement of a 51- to 59-kbp stretch between 28.9 and 29 Mbp in the Bala genome, resulting in the deletion of two cytochrome P450 genes-SLB1 and SLB2-with high homology to the Arabidopsis SL biosynthesis gene, MAX1. Both rice genes rescue the Arabidopsis max1-1 highly branched mutant phenotype and increase the production of the SL, ent-2'-epi-5-deoxystrigol, when overexpressed in Bala. Furthermore, analysis of this region in 367 cultivars of the publicly available Rice Diversity Panel population shows that the rearrangement at this locus is a recurrent natural trait associated with the Indica/Japonica divide in rice.",

keywords = "QTL, plant hormone, CYP450, Arbuscular mycorrhizal fungi, Quantitative Trait Loci, Tiller Bud Outgrowth, Striga-Hermonthica, Oryza-Sativa, Phosphate deficiency, Root morphology, Arabidopsis, Architecture, INHIBITION",

author = "Catarina Cardoso and Yanxia Zhang and Muhammad Jamil and Jo Hepworth and Tatsiana Charnikhova and Dimkpa, {Stanley O. N.} and Caroline Meharg and Wright, {Mark H.} and Junwei Liu and Xiangbing Meng and Yonghong Wang and Jiayang Li and McCouch, {Susan R.} and Ottoline Leyser and Price, {Adam H.} and Bouwmeester, {Harro J.} and Carolien Ruyter-Spira",

note = "Acknowledgments We thank Koichi Yoneyama (Utsunomiya University, Japan), Yukihiro Sugimoto (Kobe University, Japan), and Tadao Asami (University of Tokyo, Japan) for the kind provision of ent-2′-epi-orobanchol, orobanchol, 5-deoxystrigol, 2′-epi-5-deoxystrigol, and [2H]6-2′-epi-5-deoxystrigol; and Binne Zwanenburg (University of Nijmegen, The Netherlands) for providing GR24. A.H.P. and H.J.B. thank Pieter Ouwerkerk for bringing them together. This work was supported by the Higher Education Commission Pakistan (to M.J.); Netherlands Organization for Scientific Research Vici Grant 865.06.002 (to H.J.B.) and Equipment Grant 834.08.001 (to H.J.B.); the Centre for BioSystems Genomics, part of the Netherlands Genomics Initiative/Netherlands Organisation for Scientific Research (to H.J.B.); National Science Foundation Plant Genome Research Grant 1026555 (to S.R.M.); US Department of Agriculture National Institute for Food and Agriculture Grant 2009-65300-05661 (to S.R.M.); United Kingdom Biotechnology and Biological Science Research Council (to J.H.); Government of the Rivers State of Nigeria Postgraduate Scholarship (to S.O.N.D.); and National Natural Science Foundation of China Grant 31161130535 (to Y.W.). Bala sequencing was supported by European Union FP6 Project 015468 (“CEDROME”) and a Monitoring Agricultural Resources grant; Azucena sequencing was supported by Biotechnology and Biological Sciences Research Council–Department for International Development Grant BBF0041841.",

year = "2014",

month = feb,

day = "11",

doi = "10.1073/pnas.1317360111",

language = "English",

volume = "111",

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journal = "PNAS",

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TY - JOUR

T1 - Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs

AU - Cardoso, Catarina

AU - Zhang, Yanxia

AU - Jamil, Muhammad

AU - Hepworth, Jo

AU - Charnikhova, Tatsiana

AU - Dimkpa, Stanley O. N.

AU - Meharg, Caroline

AU - Wright, Mark H.

AU - Liu, Junwei

AU - Meng, Xiangbing

AU - Wang, Yonghong

AU - Li, Jiayang

AU - McCouch, Susan R.

AU - Leyser, Ottoline

AU - Price, Adam H.

AU - Bouwmeester, Harro J.

AU - Ruyter-Spira, Carolien

N1 - Acknowledgments We thank Koichi Yoneyama (Utsunomiya University, Japan), Yukihiro Sugimoto (Kobe University, Japan), and Tadao Asami (University of Tokyo, Japan) for the kind provision of ent-2′-epi-orobanchol, orobanchol, 5-deoxystrigol, 2′-epi-5-deoxystrigol, and [2H]6-2′-epi-5-deoxystrigol; and Binne Zwanenburg (University of Nijmegen, The Netherlands) for providing GR24. A.H.P. and H.J.B. thank Pieter Ouwerkerk for bringing them together. This work was supported by the Higher Education Commission Pakistan (to M.J.); Netherlands Organization for Scientific Research Vici Grant 865.06.002 (to H.J.B.) and Equipment Grant 834.08.001 (to H.J.B.); the Centre for BioSystems Genomics, part of the Netherlands Genomics Initiative/Netherlands Organisation for Scientific Research (to H.J.B.); National Science Foundation Plant Genome Research Grant 1026555 (to S.R.M.); US Department of Agriculture National Institute for Food and Agriculture Grant 2009-65300-05661 (to S.R.M.); United Kingdom Biotechnology and Biological Science Research Council (to J.H.); Government of the Rivers State of Nigeria Postgraduate Scholarship (to S.O.N.D.); and National Natural Science Foundation of China Grant 31161130535 (to Y.W.). Bala sequencing was supported by European Union FP6 Project 015468 (“CEDROME”) and a Monitoring Agricultural Resources grant; Azucena sequencing was supported by Biotechnology and Biological Sciences Research Council–Department for International Development Grant BBF0041841.

PY - 2014/2/11

Y1 - 2014/2/11

N2 - Rice (Oryza sativa) cultivar Azucena-belonging to the Japonica subspecies-exudes high strigolactone (SL) levels and induces high germination of the root parasitic plant Striga hermonthica. Consistent with the fact that SLs also inhibit shoot branching, Azucena is a low-tillering variety. In contrast, Bala, an Indica cultivar, is a low-SL producer, stimulates less Striga germination, and is highly tillered. Using a Bala x Azucena F6 population, a major quantitative trait loci-qSLB1.1- for the exudation of SL, tillering, and induction of Striga germination was detected on chromosome 1. Sequence analysis of the corresponding locus revealed a rearrangement of a 51- to 59-kbp stretch between 28.9 and 29 Mbp in the Bala genome, resulting in the deletion of two cytochrome P450 genes-SLB1 and SLB2-with high homology to the Arabidopsis SL biosynthesis gene, MAX1. Both rice genes rescue the Arabidopsis max1-1 highly branched mutant phenotype and increase the production of the SL, ent-2'-epi-5-deoxystrigol, when overexpressed in Bala. Furthermore, analysis of this region in 367 cultivars of the publicly available Rice Diversity Panel population shows that the rearrangement at this locus is a recurrent natural trait associated with the Indica/Japonica divide in rice.

AB - Rice (Oryza sativa) cultivar Azucena-belonging to the Japonica subspecies-exudes high strigolactone (SL) levels and induces high germination of the root parasitic plant Striga hermonthica. Consistent with the fact that SLs also inhibit shoot branching, Azucena is a low-tillering variety. In contrast, Bala, an Indica cultivar, is a low-SL producer, stimulates less Striga germination, and is highly tillered. Using a Bala x Azucena F6 population, a major quantitative trait loci-qSLB1.1- for the exudation of SL, tillering, and induction of Striga germination was detected on chromosome 1. Sequence analysis of the corresponding locus revealed a rearrangement of a 51- to 59-kbp stretch between 28.9 and 29 Mbp in the Bala genome, resulting in the deletion of two cytochrome P450 genes-SLB1 and SLB2-with high homology to the Arabidopsis SL biosynthesis gene, MAX1. Both rice genes rescue the Arabidopsis max1-1 highly branched mutant phenotype and increase the production of the SL, ent-2'-epi-5-deoxystrigol, when overexpressed in Bala. Furthermore, analysis of this region in 367 cultivars of the publicly available Rice Diversity Panel population shows that the rearrangement at this locus is a recurrent natural trait associated with the Indica/Japonica divide in rice.

KW - QTL

KW - plant hormone

KW - CYP450

KW - Arbuscular mycorrhizal fungi

KW - Quantitative Trait Loci

KW - Tiller Bud Outgrowth

KW - Striga-Hermonthica

KW - Oryza-Sativa

KW - Phosphate deficiency

KW - Root morphology

KW - Arabidopsis

KW - Architecture

KW - INHIBITION

U2 - 10.1073/pnas.1317360111

DO - 10.1073/pnas.1317360111

M3 - Article

SN - 0027-8424

VL - 111

SP - 2379

EP - 2384

JO - PNAS

JF - PNAS

IS - 6

ER -

Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs

Abstract

Bibliographical note

Keywords

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