Home LiteratureArticle Details
PMID: 17577400 Published · epublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice.

BMC genomics ·Vol. 8 ·2007-06-18 ·Pages 175

Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG

Abstract

Plants respond to low temperature through an intricately coordinated transcriptional network. The CBF/DREB-regulated network of genes has been shown to play a prominent role in freeze-tolerance of Arabidopsis through the process of cold acclimation (CA). Recent evidence also showed that the CBF/DREB regulon is not unique to CA but evolutionarily conserved between chilling-insensitive (temperate) and chilling-sensitive (warm-season) plants. In this study, the wide contrast in chilling sensitivity between indica and japonica rice was used as model to identify other regulatory clusters by integrative analysis of promoter architecture (ab initio) and gene expression profiles. Transcriptome analysis in chilling tolerant japonica rice identified a subset of 121 'early response' genes that were upregulated during the initial 24 hours at 10 degrees C. Among this group were four transcription factors including ROS-bZIP1 and another larger sub-group with a common feature of having as1/ocs-like elements in their promoters. Cold-induction of ROS-bZIP1 preceded the induction of as1/ocs-like element-containing genes and they were also induced by exogenous H2O2 at ambient temperature. Coordinated expression patterns and similar promoter architectures among the 'early response' genes suggest that they belong to a potential regulon (ROS-bZIP-as1/ocs regulatory module) that responds to elevated levels of ROS during chilling stress. Cultivar-specific expression signatures of the candidate genes indicate a positive correlation between the activity of the putative regulon and genotypic variation in chilling tolerance. A hypothetical model of an ROS-mediated regulon (ROS-bZIP-as1/ocs) triggered by chilling stress was assembled in rice. Based on the current results, it appears that this regulon is independent of ABA and CBF/DREB, and that its activation has an important contribution in configuring the rapid responses of rice seedlings to chilling stress.

MeSH Terms
Base Sequence Cold Temperature Gene Expression Profiling Gene Expression Regulation, Plant Genes, Plant Genomics Hydrogen Peroxide/pharmacology Molecular Sequence Data Multigene Family Oryza/genetics,physiology Plant Physiological Phenomena Plant Proteins/metabolism Reactive Oxygen Species Temperature Transcription Factors/metabolism
Chemicals
Plant Proteins Reactive Oxygen Species Transcription Factors Hydrogen Peroxide
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Cheng Chen
Department of Biological Sciences, University of Maine, Orono, ME 04469, USA. [email protected] <[email protected]>
Yun Kil-Young
Ressom Habtom W
Mohanty Bijayalaxmi
Bajic Vladimir B
Jia Yulin
Yun Song Joong
de los Reyes Benildo G
References (53)
53 references, click to expand
  1. AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsis cis-regulatory elements and transcription factors.
    BMC Bioinformatics. 2003 Jun 23;4:25 PMID: 12820902
  2. DNA and redox state induced conformational changes in the DNA-binding domain of the Myb oncoprotein.
    EMBO J. 1993 Dec;12(12):4625-33 PMID: 8223472
  3. DNA binding sites: representation and discovery.
    Bioinformatics. 2000 Jan;16(1):16-23 PMID: 10812473
  4. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor.
    Nat Biotechnol. 1999 Mar;17(3):287-91 PMID: 10096298
  5. The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species.
    Plant Physiol. 2002 Nov;130(3):1516-26 PMID: 12428016
  6. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element.
    Plant J. 1999 Sep;19(6):667-77 PMID: 10571852
  7. Current advances in abscisic acid action and signalling.
    Plant Mol Biol. 1994 Dec;26(5):1557-77 PMID: 7858204
  8. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis.
    Proc Natl Acad Sci U S A. 2004 Oct 19;101(42):15243-8 PMID: 15383661
  9. Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis.
    Plant Cell. 2003 Aug;15(8):1846-58 PMID: 12897257
  10. Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures.
    Plant Physiol. 2003 Jun;132(2):893-906 PMID: 12805619
  11. Hydrogen peroxide signalling.
    Curr Opin Plant Biol. 2002 Oct;5(5):388-95 PMID: 12183176
  12. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1.
    Plant Cell. 2005 Nov;17(11):3155-75 PMID: 16214899
  13. Redox-dependent signal transduction.
    FEBS Lett. 2000 Jun 30;476(1-2):52-4 PMID: 10878249
  14. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis.
    Plant J. 1998 Oct;16(2):223-33 PMID: 9839467
  15. PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:571-599 PMID: 15012220
  16. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system.
    J Exp Bot. 2002 May;53(372):1367-76 PMID: 11997382
  17. Production of reactive oxygen species by plant NADPH oxidases.
    Plant Physiol. 2006 Jun;141(2):336-40 PMID: 16760484
  18. The AP2/EREBP family of plant transcription factors.
    Biol Chem. 1998 Jun;379(6):633-46 PMID: 9687012
  19. Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis.
    Plant Physiol. 2006 Aug;141(4):1219-32 PMID: 16896234
  20. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis.
    Plant J. 2005 Jan;41(2):195-211 PMID: 15634197
  21. Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants.
    Mol Gen Genet. 1993 Jan;236(2-3):331-40 PMID: 8437577
  22. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.
    Curr Opin Plant Biol. 2000 Jun;3(3):217-23 PMID: 10837265
  23. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway.
    Plant Cell. 2002 Aug;14(8):1675-90 PMID: 12172015
  24. RF2b, a rice bZIP transcription activator, interacts with RF2a and is involved in symptom development of rice tungro disease.
    Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):687-92 PMID: 14704272
  25. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.
    Plant Physiol. 2003 Dec;133(4):1755-67 PMID: 14645724
  26. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1035-40 PMID: 9023378
  27. The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature.
    Gene. 2005 Jan 3;344:171-80 PMID: 15656983
  28. Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis.
    Physiol Genomics. 2004 Apr 13;17(2):87-100 PMID: 14982972
  29. bZIP transcription factors in Arabidopsis.
    Trends Plant Sci. 2002 Mar;7(3):106-11 PMID: 11906833
  30. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba.
    Plant Physiol. 2001 Aug;126(4):1438-48 PMID: 11500543
  31. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2940-5 PMID: 10717008
  32. Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells.
    Trends Plant Sci. 2001 Apr;6(4):145-50 PMID: 11286918
  33. A snapshot of the low temperature stress transcriptome of developing rice seedlings (Oryza sativa L.) via ESTs from subtracted cDNA library.
    Theor Appl Genet. 2003 Oct;107(6):1071-82 PMID: 12827255
  34. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance.
    Science. 1998 Apr 3;280(5360):104-6 PMID: 9525853
  35. RF2a, a bZIP transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development.
    EMBO J. 1997 Sep 1;16(17):5247-59 PMID: 9311985
  36. Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants.
    Plant J. 2004 Jan;37(1):115-27 PMID: 14675437
  37. LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase.
    EMBO J. 2002 Jun 3;21(11):2692-702 PMID: 12032082
  38. Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance.
    Plant Cell. 2003 Nov;15(11):2647-53 PMID: 14576289
  39. Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh.
    Plant Mol Biol. 1993 Feb;21(4):641-53 PMID: 8448363
  40. H2O2 sensing through oxidation of the Yap1 transcription factor.
    EMBO J. 2000 Oct 2;19(19):5157-66 PMID: 11013218
  41. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.
    Plant Cell. 1998 Aug;10(8):1391-406 PMID: 9707537
  42. TRANSFAC: transcriptional regulation, from patterns to profiles.
    Nucleic Acids Res. 2003 Jan 1;31(1):374-8 PMID: 12520026
  43. Regulation of the Arabidopsis transcriptome by oxidative stress.
    Plant Physiol. 2001 Sep;127(1):159-72 PMID: 11553744
  44. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation.
    Plant Cell. 1996 Mar;8(3):489-503 PMID: 8721751
  45. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation.
    Plant Physiol. 2000 Dec;124(4):1854-65 PMID: 11115899
  46. WRKY transcription factors: from DNA binding towards biological function.
    Curr Opin Plant Biol. 2004 Oct;7(5):491-8 PMID: 15337090
  47. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression.
    Plant J. 2003 Feb;33(4):751-63 PMID: 12609047
  48. Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13404-9 PMID: 11038526
  49. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate.
    Plant Cell. 2001 Jan;13(1):179-91 PMID: 11158538
  50. Plant cis-acting regulatory DNA elements (PLACE) database: 1999.
    Nucleic Acids Res. 1999 Jan 1;27(1):297-300 PMID: 9847208
  51. MEME: discovering and analyzing DNA and protein sequence motifs.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W369-73 PMID: 16845028
  52. Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley.
    Plant Mol Biol. 2004 May;55(3):399-416 PMID: 15604689
  53. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis.
    Plant J. 2004 Sep;39(6):905-19 PMID: 15341633
Article Info
Journal
BMC genomics
Abbr.
BMC Genomics
ISSN
1471-2164
Published
2007-06-18
Epub
2007-00-18
Pages
175
Language
English
Region
England
NLM ID
100965258
PMCID
PMC1925099
Subset
IM
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]