Home LiteratureArticle Details
PMID: 19029881 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids.

Nature ·Vol. 457 ·No. 7227 ·2009-01-15 ·Pages 327-31

Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ

Abstract

Segregating hybrids and stable allopolyploids display morphological vigour, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and Arabidopsis arenosa-the mechanisms for this are unknown. Circadian clocks mediate metabolic pathways and increase fitness in animals and plants. Here we report that epigenetic modifications of the circadian clock genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) and their reciprocal regulators TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI) mediate expression changes in downstream genes and pathways. During the day, epigenetic repression of CCA1 and LHY induced the expression of TOC1, GI and downstream genes containing evening elements in chlorophyll and starch metabolic pathways in allotetraploids and F(1) hybrids, which produced more chlorophyll and starch than the parents in the same environment. Mutations in cca1 and cca1 lhy and the daily repression of cca1 by RNA interference (RNAi) in TOC1::cca1(RNAi) transgenic plants increased the expression of downstream genes and increased chlorophyll and starch content, whereas constitutively expressing CCA1 or ectopically expressing TOC1::CCA1 had the opposite effect. The causal effects of CCA1 on output traits suggest that hybrids and allopolyploids gain advantages from the control of circadian-mediated physiological and metabolic pathways, leading to growth vigour and increased biomass.

MeSH Terms
Arabidopsis/classification,genetics,growth & development Arabidopsis Proteins/genetics,metabolism Base Sequence Biological Clocks/genetics,physiology Chlorophyll/metabolism Chromatin/genetics Circadian Rhythm/genetics,physiology DNA-Binding Proteins/genetics,metabolism Epigenesis, Genetic Gene Expression Regulation, Plant/genetics Hybridization, Genetic Plants, Genetically Modified Polyploidy Starch/biosynthesis Transcription Factors/genetics,metabolism
Chemicals
Arabidopsis Proteins CCA1 protein, Arabidopsis Chromatin DNA-Binding Proteins GI protein, Arabidopsis LHY protein, Arabidopsis TOC1 protein, Arabidopsis Transcription Factors Chlorophyll Starch
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Ni Zhongfu
Section of Molecular Cell and Developmental Biology, The University of Texas at Austin, One University Station, A-4800, Austin, Texas 78712, USA.
Kim Eun-Deok
Ha Misook
Lackey Erika
Liu Jianxin
Zhang Yirong
Sun Qixin
Chen Z Jeffrey
References (42)
42 references, click to expand
  1. Phenotypic instability and rapid gene silencing in newly formed arabidopsis allotetraploids.
    Plant Cell. 2000 Sep;12(9):1551-68 PMID: 11006331
  2. Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development.
    Genetics. 2005 Jan;169(1):337-45 PMID: 15371352
  3. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene.
    Science. 1999 Sep 3;285(5433):1579-82 PMID: 10477524
  4. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids.
    Genetics. 2006 Jan;172(1):507-17 PMID: 16172500
  5. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis.
    Dev Cell. 2002 May;2(5):629-41 PMID: 12015970
  6. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):2053-8 PMID: 11172074
  7. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids.
    Annu Rev Plant Biol. 2007;58:377-406 PMID: 17280525
  8. Enhanced fitness conferred by naturally occurring variation in the circadian clock.
    Science. 2003 Nov 7;302(5647):1049-53 PMID: 14605371
  9. Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids.
    Genetics. 2006 Jun;173(2):965-74 PMID: 16547097
  10. The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter.
    Plant Cell. 2001 Aug;13(8):1907-18 PMID: 11487701
  11. PORA and PORB, Two Light-Dependent Protochlorophyllide-Reducing Enzymes of Angiosperm Chlorophyll Biosynthesis.
    Plant Cell. 1996 May;8(5):763-769 PMID: 12239398
  12. Quantification of starch in plant tissues.
    Nat Protoc. 2006;1(3):1342-5 PMID: 17406420
  13. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression.
    Cell. 1998 Jun 26;93(7):1207-17 PMID: 9657153
  14. Monogenic Recessive Mutations Causing Both Late Floral Initiation and Excess Starch Accumulation in Arabidopsis.
    Plant Cell. 1995 Oct;7(10):1703-1712 PMID: 12242359
  15. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana.
    Nature. 2002 Sep 5;419(6902):74-7 PMID: 12214234
  16. The TIME FOR COFFEE gene maintains the amplitude and timing of Arabidopsis circadian clocks.
    Plant Cell. 2003 Nov;15(11):2719-29 PMID: 14555691
  17. Plant speciation.
    Science. 2007 Aug 17;317(5840):910-4 PMID: 17702935
  18. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  19. Genomic plasticity and the diversity of polyploid plants.
    Science. 2008 Apr 25;320(5875):481-3 PMID: 18436776
  20. Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis.
    Curr Biol. 2002 Apr 30;12(9):757-61 PMID: 12007421
  21. In search of the molecular basis of heterosis.
    Plant Cell. 2003 Oct;15(10):2236-9 PMID: 14523245
  22. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.
    Science. 2000 Dec 15;290(5499):2110-3 PMID: 11118138
  23. Interplay of circadian clocks and metabolic rhythms.
    Annu Rev Genet. 2006;40:409-48 PMID: 17094740
  24. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  25. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  26. wrinkled1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism.
    Plant Physiol. 1998 Sep;118(1):91-101 PMID: 9733529
  27. Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids.
    Plant Physiol. 2002 Jun;129(2):733-46 PMID: 12068115
  28. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog.
    Science. 2000 Aug 4;289(5480):768-71 PMID: 10926537
  29. Circadian rhythms from flies to human.
    Nature. 2002 May 16;417(6886):329-35 PMID: 12015613
  30. Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis.
    Plant Cell. 2005 Jul;17(7):1926-40 PMID: 15923346
  31. Leaf starch degradation comes out of the shadows.
    Trends Plant Sci. 2005 Mar;10(3):130-7 PMID: 15749471
  32. Vernalization requires epigenetic silencing of FLC by histone methylation.
    Nature. 2004 Jan 8;427(6970):164-7 PMID: 14712277
  33. Overexpression of light-dependent PORA or PORB in plants depleted of endogenous POR by far-red light enhances seedling survival in white light and protects against photooxidative damage.
    Plant J. 1997 Sep;12(3):649-58 PMID: 9351249
  34. A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock.
    Plant Cell. 2007 Jul;19(7):2111-23 PMID: 17616736
  35. Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids.
    Genetics. 2004 Aug;167(4):1961-73 PMID: 15342533
  36. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.
    Science. 2001 Aug 3;293(5531):880-3 PMID: 11486091
  37. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage.
    Science. 2005 Jul 22;309(5734):630-3 PMID: 16040710
  38. Plant circadian rhythms.
    Plant Cell. 2006 Apr;18(4):792-803 PMID: 16595397
  39. Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves.
    Plant Physiol. 2004 Sep;136(1):2687-99 PMID: 15347792
  40. Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species.
    Plant Biotechnol J. 2004 Jan;2(1):45-57 PMID: 17166142
  41. Starch degradation.
    Annu Rev Plant Biol. 2005;56:73-98 PMID: 15862090
  42. Heterosis: revisiting the magic.
    Trends Genet. 2007 Feb;23(2):60-6 PMID: 17188398
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature07523
Published
2009-01-15
Epub
2008-00-23
Pages
327-31
Language
English
Region
England
NLM ID
0410462
PMCID
PMC2679702
Subset
IM
Grants
NIGMS NIH HHS · R01 GM067015 · United States
NIGMS NIH HHS · GM067015 · United States
NIGMS NIH HHS · R01 GM067015-05 · United States
NIGMS NIH HHS · R01 GM067015-06 · United States
NIGMS NIH HHS · R01 GM067015-04 · United States
External Links
PubMed source DOI: 10.1038/nature07523 PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2