Home LiteratureArticle Details
PMID: 20130099 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A novel MYBS3-dependent pathway confers cold tolerance in rice.

Plant physiology ·Vol. 153 ·No. 1 ·2010-05-00 ·Pages 145-58

Su CF, Wang YC, Hsieh TH, Lu CA, Tseng TH, Yu SM

Abstract

Rice (Oryza sativa) seedlings are particularly sensitive to chilling in early spring in temperate and subtropical zones and in high-elevation areas. Improvement of chilling tolerance in rice may significantly increase rice production. MYBS3 is a single DNA-binding repeat MYB transcription factor previously shown to mediate sugar signaling in rice. In this study, we observed that MYBS3 also plays a critical role in cold adaptation in rice. Gain- and loss-of-function analyses indicated that MYBS3 was sufficient and necessary for enhancing cold tolerance in rice. Transgenic rice constitutively overexpressing MYBS3 tolerated 4 degrees C for at least 1 week and exhibited no yield penalty in normal field conditions. Transcription profiling of transgenic rice overexpressing or underexpressing MYBS3 led to the identification of many genes in the MYBS3-mediated cold signaling pathway. Several genes activated by MYBS3 as well as inducible by cold have previously been implicated in various abiotic stress responses and/or tolerance in rice and other plant species. Surprisingly, MYBS3 repressed the well-known DREB1/CBF-dependent cold signaling pathway in rice, and the repression appears to act at the transcriptional level. DREB1 responded quickly and transiently while MYBS3 responded slowly to cold stress, which suggests that distinct pathways act sequentially and complementarily for adapting short- and long-term cold stress in rice. Our studies thus reveal a hitherto undiscovered novel pathway that controls cold adaptation in rice.

MeSH Terms
Acclimatization Cold Temperature Gene Expression Regulation, Plant Oryza/metabolism Plant Proteins/metabolism Stress, Physiological Transcription Factors/metabolism
Chemicals
Plant Proteins Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Su Chin-Fen
Institute of Biotechnology, National Cheng Kung University, Tainan 701, Taiwan, Republic of China.
Wang Yi-Chieh
Hsieh Tsai-Hung
Lu Chung-An
Tseng Tung-Hai
Yu Su-May
References (65)
65 references, click to expand
  1. Sugar response sequence in the promoter of a rice alpha-amylase gene serves as a transcriptional enhancer.
    J Biol Chem. 1998 Apr 24;273(17):10120-31 PMID: 9553059
  2. Transcriptomic adaptations in rice suspension cells under sucrose starvation.
    Plant Mol Biol. 2007 Mar;63(4):441-63 PMID: 17115300
  3. Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):6309-14 PMID: 15079051
  4. Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes.
    Plant Physiol. 2009 May;150(1):244-56 PMID: 19279197
  5. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity.
    Plant J. 2000 Sep;23(6):785-94 PMID: 10998189
  6. Cold stress regulation of gene expression in plants.
    Trends Plant Sci. 2007 Oct;12(10):444-51 PMID: 17855156
  7. Repression of stress-responsive genes by FIERY2, a novel transcriptional regulator in Arabidopsis.
    Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10899-904 PMID: 12149453
  8. Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth.
    Plant Physiol. 2003 Feb;131(2):516-24 PMID: 12586876
  9. The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice.
    Plant Cell. 2007 Aug;19(8):2484-99 PMID: 17766403
  10. Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells.
    Plant Physiol. 2005 Jan;137(1):176-89 PMID: 15618416
  11. 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
  12. 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
  13. The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression Is regulated by low temperature but not by abscisic acid or dehydration.
    Plant Physiol. 1999 Feb;119(2):463-70 PMID: 9952441
  14. Multiple mode regulation of a cysteine proteinase gene expression in rice.
    Plant Physiol. 2000 Jan;122(1):57-66 PMID: 10631249
  15. RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance.
    Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11507-12 PMID: 12165572
  16. Evidence for Chilling-Induced Oxidative Stress in Maize Seedlings and a Regulatory Role for Hydrogen Peroxide.
    Plant Cell. 1994 Jan;6(1):65-74 PMID: 12244221
  17. 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
  18. A multidrug resistance transporter in Magnaporthe is required for host penetration and for survival during oxidative stress.
    Plant Cell. 2006 Dec;18(12):3686-705 PMID: 17189344
  19. The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family.
    Plant Mol Biol. 2006 Jan;60(1):107-24 PMID: 16463103
  20. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes.
    Curr Opin Plant Biol. 2002 Jun;5(3):250-7 PMID: 11960744
  21. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance.
    Plant Cell. 2009 Mar;21(3):972-84 PMID: 19270186
  22. Mapping of QTLs associated with cold tolerance during the vegetative stage in rice.
    J Exp Bot. 2003 Nov;54(392):2579-85 PMID: 12966040
  23. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis.
    Genes Dev. 2003 Apr 15;17(8):1043-54 PMID: 12672693
  24. PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:571-599 PMID: 15012220
  25. Membrane Fluidity and Temperature Perception.
    Plant Physiol. 1997 Nov;115(3):875-879 PMID: 12223851
  26. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):15898-903 PMID: 12456878
  27. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.
    Annu Rev Plant Biol. 2006;57:781-803 PMID: 16669782
  28. New insights on trehalose: a multifunctional molecule.
    Glycobiology. 2003 Apr;13(4):17R-27R PMID: 12626396
  29. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression.
    Plant J. 1998 Nov;16(4):433-42 PMID: 9881163
  30. Metabolic derepression of alpha-amylase gene expression in suspension-cultured cells of rice.
    J Biol Chem. 1991 Nov 5;266(31):21131-7 PMID: 1939156
  31. Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes.
    FEBS J. 2007 Mar;274(5):1192-201 PMID: 17257172
  32. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings.
    Chemosphere. 2009 Feb;74(5):688-702 PMID: 18996570
  33. CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis.
    Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3985-90 PMID: 15004278
  34. An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice.
    BMC Genomics. 2007 Jun 18;8:175 PMID: 17577400
  35. Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis.
    Plant Cell. 2003 Dec;15(12):2940-51 PMID: 14630965
  36. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice.
    Plant Cell Physiol. 2006 Jan;47(1):141-53 PMID: 16284406
  37. The root-specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis.
    Plant Mol Biol. 2004 May;55(3):315-25 PMID: 15604684
  38. Temperature sensing and cold acclimation.
    Curr Opin Plant Biol. 2001 Jun;4(3):241-6 PMID: 11312135
  39. Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens.
    BMC Plant Biol. 2008 Jun 20;8:68 PMID: 18570649
  40. Adaptations to Environmental Stresses.
    Plant Cell. 1995 Jul;7(7):1099-1111 PMID: 12242400
  41. 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
  42. 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
  43. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance.
    Science. 1998 Apr 3;280(5360):104-6 PMID: 9525853
  44. The 5'-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression.
    Plant Mol Biol. 1994 Mar;24(5):701-13 PMID: 8193295
  45. Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples.
    Plant Cell Rep. 2008 Oct;27(10):1677-86 PMID: 18679687
  46. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes.
    Planta. 2008 Jun;228(1):191-201 PMID: 18365248
  47. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress.
    Plant Cell. 1994 Feb;6(2):251-64 PMID: 8148648
  48. 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
  49. Trehalose biosynthesis in response to abiotic stresses.
    J Integr Plant Biol. 2008 Oct;50(10):1223-9 PMID: 19017109
  50. 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
  51. Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice.
    Plant Mol Biol. 2005 Aug;58(6):751-762 PMID: 16240171
  52. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana.
    Plant J. 2002 Feb;29(4):417-26 PMID: 11846875
  53. Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice.
    Plant Physiol. 2002 Aug;129(4):1880-91 PMID: 12177502
  54. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression.
    Mol Microbiol. 1993 Apr;8(2):205-10 PMID: 8391102
  55. Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of alpha-amylase gene expression.
    Plant Cell. 2002 Aug;14(8):1963-80 PMID: 12172034
  56. Binding of sulfonylurea by AtMRP5, an Arabidopsis multidrug resistance-related protein that functions in salt tolerance.
    Plant Physiol. 2004 Jan;134(1):528-38 PMID: 14684837
  57. The calcium sensor CBL1 integrates plant responses to abiotic stresses.
    Plant J. 2003 Nov;36(4):457-70 PMID: 14617077
  58. F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress.
    Plant Physiol. 2007 Apr;143(4):1467-83 PMID: 17293439
  59. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice.
    Plant J. 2007 Aug;51(4):617-30 PMID: 17587305
  60. 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
  61. 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
  62. Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants.
    Plant Biotechnol J. 2008 Jun;6(5):486-503 PMID: 18384508
  63. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo--cytoplasmic partitioning.
    Genes Dev. 2001 Apr 1;15(7):912-24 PMID: 11297514
  64. Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis.
    Plant Physiol. 2007 Apr;143(4):1739-51 PMID: 17293435
  65. An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression.
    Biochem Biophys Res Commun. 1998 Sep 8;250(1):161-70 PMID: 9735350
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2010-05-00
Epub
2010-00-03
Pages
145-58
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2862423
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]