Home LiteratureArticle Details
PMID: 17220364 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

DELLAs contribute to plant photomorphogenesis.

Plant physiology ·Vol. 143 ·No. 3 ·2007-03-00 ·Pages 1163-72

Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X, Harberd NP

Abstract

Plant morphogenesis is profoundly influenced by light (a phenomenon known as photomorphogenesis). For example, light inhibits seedling hypocotyl growth via activation of phytochromes and additional photoreceptors. Subsequently, information is transmitted through photoreceptor-linked signal transduction pathways and used (via previously unknown mechanisms) to control hypocotyl growth. Here we show that light inhibition of Arabidopsis (Arabidopsis thaliana) hypocotyl growth is in part dependent on the DELLAs (a family of nuclear growth-restraining proteins that mediate the effect of the phytohormone gibberellin [GA] on growth). We show that light inhibition of growth is reduced in DELLA-deficient mutant hypocotyls. We also show that light activation of phytochromes promotes the accumulation of DELLAs. A green fluorescent protein (GFP)-tagged DELLA (GFP-RGA) accumulates in elongating cells of light-grown, but not dark-grown, transgenic wild-type hypocotyls. Furthermore, transfer of seedlings from light to dark (or vice versa) results in rapid changes in hypocotyl GFP-RGA accumulation, changes that are paralleled by rapid alterations in the abundance in hypocotyls of transcripts encoding enzymes of GA metabolism. These observations suggest that light-dependent changes in hypocotyl GFP-RGA accumulation are a consequence of light-dependent changes in bioactive GA level. Finally, we show that GFP accumulation and quantitative modulation of hypocotyl growth is proportionate with light energy dose (the product of exposure duration and fluence rate). Hence, DELLAs inhibit hypocotyl growth during the light phase of the day-night cycle via a mechanism that is quantitatively responsive to natural light variability. We conclude that DELLAs are a major component of the adaptively significant mechanism via which light regulates plant growth during photomorphogenesis.

MeSH Terms
Arabidopsis/drug effects,growth & development,metabolism Arabidopsis Proteins/analysis,metabolism,physiology Gibberellins/pharmacology Green Fluorescent Proteins/analysis Hypocotyl/drug effects,growth & development,metabolism Light Multigene Family Photoperiod Phytochrome A/metabolism Phytochrome B/metabolism Plant Growth Regulators/pharmacology RNA, Messenger/metabolism Repressor Proteins/analysis,metabolism,physiology Signal Transduction
Chemicals
Arabidopsis Proteins Gibberellins PHYA protein, Arabidopsis PHYB protein, Arabidopsis Phytochrome A Plant Growth Regulators RGA protein, Arabidopsis RNA, Messenger Repressor Proteins Phytochrome B Green Fluorescent Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Achard Patrick
John Innes Centre, Colney, Norwich NR4 7UH, United Kingdom.
Liao Lili
Jiang Caifu
Desnos Thierry
Bartlett Joanne
Fu Xiangdong
Harberd Nicholas P
References (48)
48 references, click to expand
  1. Gibberellin deficiency and response mutations suppress the stem elongation phenotype of phytochrome-deficient mutants of Arabidopsis.
    Plant Physiol. 1997 Apr;113(4):1051-8 PMID: 9112768
  2. Light signal transduction in higher plants.
    Annu Rev Genet. 2004;38:87-117 PMID: 15568973
  3. Changes in gibberellin A(1) levels and response during de-etiolation of pea seedlings.
    Plant Physiol. 2000 Oct;124(2):805-12 PMID: 11027728
  4. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana.
    Genetics. 2001 Oct;159(2):777-85 PMID: 11606552
  5. Evidence that the Arabidopsis nuclear gibberellin signalling protein GAI is not destabilised by gibberellin.
    Plant J. 2002 Dec;32(6):935-47 PMID: 12492836
  6. Identification and characterization of Arabidopsis gibberellin receptors.
    Plant J. 2006 Jun;46(5):880-9 PMID: 16709201
  7. Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis.
    Plant Physiol. 1995 Jul;108(3):1049-57 PMID: 7630935
  8. Derivative Alleles of the Arabidopsis Gibberellin-Insensitive (gai) Mutation Confer a Wild-Type Phenotype.
    Plant Cell. 1993 Mar;5(3):351-360 PMID: 12271067
  9. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation.
    Plant Cell. 2004 Jun;16(6):1392-405 PMID: 15155881
  10. Phytochrome photosensory signalling networks.
    Nat Rev Mol Cell Biol. 2002 Feb;3(2):85-93 PMID: 11836510
  11. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light.
    Plant Cell. 1993 Jul;5(7):757-68 PMID: 8364355
  12. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway.
    Plant Cell. 1998 Feb;10(2):155-69 PMID: 9490740
  13. The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis.
    Plant Cell. 1994 Oct;6(10):1509-18 PMID: 7994182
  14. Isolation of the Arabidopsis GA4 locus.
    Plant Cell. 1995 Feb;7(2):195-201 PMID: 7756830
  15. 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
  16. Auxin promotes Arabidopsis root growth by modulating gibberellin response.
    Nature. 2003 Feb 13;421(6924):740-3 PMID: 12610625
  17. FHY1: a phytochrome A-specific signal transducer.
    Genes Dev. 2001 Nov 15;15(22):2980-90 PMID: 11711433
  18. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase.
    Plant Cell. 2003 May;15(5):1120-30 PMID: 12724538
  19. Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis.
    Plant Cell. 1999 May;11(5):927-36 PMID: 10330476
  20. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis.
    Plant Cell. 2001 Jul;13(7):1555-66 PMID: 11449051
  21. Gibberellin dose-response regulation of GA4 gene transcript levels in Arabidopsis.
    Plant Physiol. 1998 Aug;117(4):1195-203 PMID: 9701576
  22. Phytochrome B affects responsiveness to gibberellins in Arabidopsis.
    Plant Physiol. 1996 Sep;112(1):337-42 PMID: 8819329
  23. Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12771-6 PMID: 15308775
  24. Gibberellins repress photomorphogenesis in darkness.
    Plant Physiol. 2004 Mar;134(3):1050-7 PMID: 14963246
  25. Cloning the Arabidopsis GA1 Locus by Genomic Subtraction.
    Plant Cell. 1992 Feb;4(2):119-128 PMID: 12297643
  26. Regulation of gibberellin 20-oxidase and gibberellin 3beta-hydroxylase transcript accumulation during De-etiolation of pea seedlings.
    Plant Physiol. 1999 Nov;121(3):783-91 PMID: 10557226
  27. HOW GIBBERELLIN REGULATES PLANT GROWTH AND DEVELOPMENT: A Molecular Genetic Analysis of Gibberellin Signaling.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:67-88 PMID: 11337392
  28. Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis.
    Plant Physiol. 2004 Jun;135(2):1008-19 PMID: 15173565
  29. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development.
    Plant Cell. 1993 Feb;5(2):147-57 PMID: 8453299
  30. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function.
    Development. 2004 Mar;131(5):1055-64 PMID: 14973286
  31. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant.
    Science. 2003 Mar 21;299(5614):1896-8 PMID: 12649483
  32. Integration of plant responses to environmentally activated phytohormonal signals.
    Science. 2006 Jan 6;311(5757):91-4 PMID: 16400150
  33. Ethylene regulates arabidopsis development via the modulation of DELLA protein growth repressor function.
    Plant Cell. 2003 Dec;15(12):2816-25 PMID: 14615596
  34. Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A.
    Plant Physiol. 1993 May;102(1):269-277 PMID: 12231818
  35. Gibberellin: inhibitor of an inhibitor of...?
    Bioessays. 1998 Dec;20(12):1001-8 PMID: 10048300
  36. Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA.
    Genetics. 2001 Oct;159(2):767-76 PMID: 11606551
  37. The role of GRAS proteins in plant signal transduction and development.
    Planta. 2004 Mar;218(5):683-92 PMID: 14760535
  38. The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates.
    Plant Cell. 2004 Jun;16(6):1406-18 PMID: 15161962
  39. Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition.
    Genes Dev. 2002 Mar 1;16(5):646-58 PMID: 11877383
  40. Botany. Relieving DELLA restraint.
    Science. 2003 Mar 21;299(5614):1853-4 PMID: 12649470
  41. Floral homeotic genes are targets of gibberellin signaling in flower development.
    Proc Natl Acad Sci U S A. 2004 May 18;101(20):7827-32 PMID: 15128937
  42. Photoresponses of Light-Grown phyA Mutants of Arabidopsis (Phytochrome A Is Required for the Perception of Daylength Extensions).
    Plant Physiol. 1994 May;105(1):141-149 PMID: 12232194
  43. Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis.
    Planta. 2005 Dec;223(1):105-13 PMID: 16034591
  44. Arabidopsis RGL1 encodes a negative regulator of gibberellin responses.
    Plant Cell. 2002 Jan;14(1):87-100 PMID: 11826301
  45. Phytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds.
    Plant Cell. 1998 Dec;10(12):2115-26 PMID: 9836749
  46. Arabidopsis HY8 locus encodes phytochrome A.
    Plant Cell. 1993 Sep;5(9):1081-8 PMID: 8400877
  47. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses.
    Genes Dev. 1997 Dec 1;11(23):3194-205 PMID: 9389651
  48. Light Regulation of Gibberellin Biosynthesis and Mode of Action.
    J Plant Growth Regul. 2001 Dec;20(4):354-368 PMID: 11986761
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2007-03-00
Epub
2007-00-12
Pages
1163-72
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC1820925
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/E/J/00000583 · United Kingdom
Biotechnology and Biological Sciences Research Council · P19972 · United Kingdom
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]