Home LiteratureArticle Details
PMID: 16399803 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice.

The Plant cell ·Vol. 18 ·No. 2 ·2006-02-00 ·Pages 442-56

Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z

Abstract

The recessive tall rice (Oryza sativa) mutant elongated uppermost internode (eui) is morphologically normal until its final internode elongates drastically at the heading stage. The stage-specific developmental effect of the eui mutation has been used in the breeding of hybrid rice to improve the performance of heading in male sterile cultivars. We found that the eui mutant accumulated exceptionally large amounts of biologically active gibberellins (GAs) in the uppermost internode. Map-based cloning revealed that the Eui gene encodes a previously uncharacterized cytochrome P450 monooxygenase, CYP714D1. Using heterologous expression in yeast, we found that EUI catalyzed 16alpha,17-epoxidation of non-13-hydroxylated GAs. Consistent with the tall and dwarfed phenotypes of the eui mutant and Eui-overexpressing transgenic plants, respectively, 16alpha,17-epoxidation reduced the biological activity of GA(4) in rice, demonstrating that EUI functions as a GA-deactivating enzyme. Expression of Eui appeared tightly regulated during plant development, in agreement with the stage-specific eui phenotypes. These results indicate the existence of an unrecognized pathway for GA deactivation by EUI during the growth of wild-type internodes. The identification of Eui as a GA catabolism gene provides additional evidence that the GA metabolism pathway is a useful target for increasing the agronomic value of crops.

MeSH Terms
Catalysis Cytochrome P-450 Enzyme System/genetics,metabolism Endoplasmic Reticulum/metabolism,ultrastructure Gene Expression Gene Expression Regulation, Developmental Gibberellins/biosynthesis,chemistry,metabolism Mixed Function Oxygenases Molecular Sequence Data Mutation/genetics Oryza/enzymology,genetics,metabolism Phenotype Phylogeny Physical Chromosome Mapping Plant Proteins/genetics,metabolism Plants, Genetically Modified/anatomy & histology Protein Transport
Chemicals
Gibberellins Plant Proteins Cytochrome P-450 Enzyme System Mixed Function Oxygenases
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Zhu Yongyou
National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
Nomura Takahito
Xu Yonghan
Zhang Yingying
Peng Yu
Mao Bizeng
Hanada Atsushi
Zhou Haicheng
Wang Renxiao
Li Peijin
Zhu Xudong
Mander Lewis N
Kamiya Yuji
Yamaguchi Shinjiro
He Zuhua
References (37)
37 references, click to expand
  1. Green revolution: a mutant gibberellin-synthesis gene in rice.
    Nature. 2002 Apr 18;416(6882):701-2 PMID: 11961544
  2. Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11638-43 PMID: 11027362
  3. Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants?
    Plant J. 2003 Jul;35(1):104-15 PMID: 12834406
  4. Functional genomics of P450s.
    Annu Rev Plant Biol. 2003;54:629-67 PMID: 14503006
  5. FMDV-2A sequence and protein arrangement contribute to functionality of CYP2B1-reporter fusion protein.
    Anal Biochem. 2005 Aug 1;343(1):116-24 PMID: 15955524
  6. slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8.
    Plant Cell. 2001 May;13(5):999-1010 PMID: 11340177
  7. Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis.
    Plant Physiol. 1999 Feb;119(2):507-10 PMID: 9952446
  8. A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase.
    Plant Mol Biol. 2004 Mar;54(4):533-47 PMID: 15316288
  9. Gibberellin metabolism: new insights revealed by the genes.
    Trends Plant Sci. 2000 Dec;5(12):523-30 PMID: 11120474
  10. Molecular mechanism of gibberellin signaling in plants.
    Annu Rev Plant Biol. 2004;55:197-223 PMID: 15377219
  11. The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):2065-70 PMID: 11172076
  12. Endogenous Gibberellins from Sporophytes of Two Tree Ferns, Cibotium glaucum and Dicksonia antarctica.
    Plant Physiol. 1988 Mar;86(3):857-62 PMID: 16666000
  13. Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4698-703 PMID: 10200325
  14. 'Green revolution' genes encode mutant gibberellin response modulators.
    Nature. 1999 Jul 15;400(6741):256-61 PMID: 10421366
  15. Gibberellins in seedlings and flowering trees of Prunus avium L.
    Phytochemistry. 2000 Feb;53(4):519-28 PMID: 10731033
  16. Sanguinarine biosynthesis is associated with the endoplasmic reticulum in cultured opium poppy cells after elicitor treatment.
    Plant Physiol. 2005 May;138(1):173-83 PMID: 15849302
  17. Gibberellin signaling: biosynthesis, catabolism, and response pathways.
    Plant Cell. 2002;14 Suppl:S61-80 PMID: 12045270
  18. Identification of a 98-kb DNA segment containing the rice Eui gene controlling uppermost internode elongation, and construction of a TAC transgene sublibrary.
    Mol Genet Genomics. 2004 Sep;272(2):149-55 PMID: 15338279
  19. Induction of H2O2 in transgenic rice leads to cell death and enhanced resistance to both bacterial and fungal pathogens.
    Transgenic Res. 2003 Oct;12(5):577-86 PMID: 14601656
  20. Semidwarf (sd-1), "green revolution" rice, contains a defective gibberellin 20-oxidase gene.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):9043-8 PMID: 12077303
  21. Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot.
    Plant Physiol. 2004 Jun;135(2):756-72 PMID: 15208422
  22. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  23. Yeast expression of animal and plant P450s in optimized redox environments.
    Methods Enzymol. 1996;272:51-64 PMID: 8791762
  24. Inhibition of gibberellin-induced elongation growth of rice by feruloyl oligosaccharides.
    Plant Cell Physiol. 1995 Dec;36(8):1447-51 PMID: 8589928
  25. An overview of gibberellin metabolism enzyme genes and their related mutants in rice.
    Plant Physiol. 2004 Apr;134(4):1642-53 PMID: 15075394
  26. Gibberellins in shoots and developing capsules of Populus species.
    Phytochemistry. 2002 Mar;59(6):679-87 PMID: 11867101
  27. A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway.
    Plant J. 2001 Oct;28(2):201-8 PMID: 11722763
  28. Gibberellin 2-oxidation and the SLN gene of Pisum sativum.
    Plant J. 1999 Jul;19(1):65-73 PMID: 10417727
  29. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant.
    Science. 2003 Mar 21;299(5614):1896-8 PMID: 12649483
  30. Gibberellin biosynthesis: its regulation by endogenous and environmental signals.
    Plant Cell Physiol. 2000 Mar;41(3):251-7 PMID: 10805587
  31. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin.
    Nature. 2005 Sep 29;437(7059):693-8 PMID: 16193045
  32. Metabolism and Biological Activity of Gibberellin A4 in Vegetative Shoots of Zea mays, Oryza sativa, and Arabidopsis thaliana.
    Plant Physiol. 1993 Jun;102(2):379-386 PMID: 12231829
  33. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment.
    Brief Bioinform. 2004 Jun;5(2):150-63 PMID: 15260895
  34. Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants.
    Plant Cell. 2003 Jan;15(1):151-63 PMID: 12509528
  35. Plant nuclei can contain extensive grooves and invaginations.
    Plant Cell. 2000 Dec;12(12):2425-2440 PMID: 11148288
  36. Phytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds.
    Plant Cell. 1998 Dec;10(12):2115-26 PMID: 9836749
  37. Molecular cloning of GA 2-oxidase3 from spinach and its ectopic expression in Nicotiana sylvestris.
    Plant Physiol. 2005 May;138(1):243-54 PMID: 15821147
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2006-02-00
Epub
2006-00-06
Pages
442-56
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1356550
Subset
IM
Databases
GENBANK
AY987039, AY987040, DQ004852, DQ004853
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]