First published online July 16, 2004; 10.1105/tpc.104.022830
The Plant Cell 16:2001-2019 (2004)
© 2004 American Society of Plant Biologists
Novel and Stress-Regulated MicroRNAs and Other Small RNAs from Arabidopsis
Ramanjulu Sunkar and
Jian-Kang Zhu1
Institute for Integrative Genome Biology and Department of Botany and Plant Sciences, University of California, Riverside, California 92521
1 To whom correspondence should be addressed. E-mail jian-kang.zhu{at}ucr.edu; fax 909-827-7115.
MicroRNAs (miRNAs) and short interfering RNAs (siRNAs) are small noncoding RNAs that have recently emerged as important regulators of mRNA degradation, translational repression, and chromatin modification. In Arabidopsis thaliana, 43 miRNAs comprising 15 families have been reported thus far. In an attempt to identify novel and abiotic stress regulated miRNAs and siRNAs, we constructed a library of small RNAs from Arabidopsis seedlings exposed to dehydration, salinity, or cold stress or to the plant stress hormone abscisic acid. Sequencing of the library and subsequent analysis revealed 26 new miRNAs from 34 loci, forming 15 new families. Two of the new miRNAs from three loci are members of previously reported miR171 and miR319 families. Some of the miRNAs are preferentially expressed in specific tissues, and several are either upregulated or downregulated by abiotic stresses. Ten of the miRNAs are highly conserved in other plant species. Fifty-one potential targets with diverse function were predicted for the newly identified miRNAs based on sequence complementarity. In addition to miRNAs, we identified 102 other novel endogenous small RNAs in Arabidopsis. These findings suggest that a large number of miRNAs and other small regulatory RNAs are encoded by the Arabidopsis genome and that some of them may play important roles in plant responses to environmental stresses as well as in development and genome maintenance.
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|
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|
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|

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|
 |
|

|
 |

|
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|
 |
|

|
 |

|
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146(4):
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|
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|

|
 |

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105(12):
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|
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|

|
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|

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|
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|
 |
|

|
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|
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S. Katiyar-Agarwal, S. Gao, A. Vivian-Smith, and H. Jin
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11768 - 11780.
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|
 |
|

|
 |

|
 |
 
R. Narsai, K. A. Howell, A. H. Millar, N. O'Toole, I. Small, and J. Whelan
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|
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|

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145(3):
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|
 |
|

|
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|
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|
 |
|

|
 |

|
 |
 
H. Yamasaki, S. E. Abdel-Ghany, C. M. Cohu, Y. Kobayashi, T. Shikanai, and M. Pilon
Regulation of Copper Homeostasis by Micro-RNA in Arabidopsis
J. Biol. Chem.,
June 1, 2007;
282(22):
16369 - 16378.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Tesfaye, J. Liu, D. L. Allan, and C. P. Vance
Genomic and Genetic Control of Phosphate Stress in Legumes
Plant Physiology,
June 1, 2007;
144(2):
594 - 603.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Zhu and C. R. Buell
Improvement of whole-genome annotation of cereals through comparative analyses
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March 1, 2007;
17(3):
299 - 310.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. D. Howell, N. Fahlgren, E. J. Chapman, J. S. Cumbie, C. M. Sullivan, S. A. Givan, K. D. Kasschau, and J. C. Carrington
Genome-Wide Analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 Pathway in Arabidopsis Reveals Dependency on miRNA- and tasiRNA-Directed Targeting
PLANT CELL,
March 1, 2007;
19(3):
926 - 942.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Rajagopalan, H. Vaucheret, J. Trejo, and D. P. Bartel
A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana
Genes & Dev.,
December 15, 2006;
20(24):
3407 - 3425.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Bove, C. L.H. Hord, and M. A. Mullen
The blossoming of RNA biology: Novel insights from plant systems
RNA,
December 1, 2006;
12(12):
2035 - 2046.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Arteaga-Vazquez, J. Caballero-Perez, and J.-P. Vielle-Calzada
A Family of MicroRNAs Present in Plants and Animals
PLANT CELL,
December 1, 2006;
18(12):
3355 - 3369.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Katiyar-Agarwal, R. Morgan, D. Dahlbeck, O. Borsani, A. Villegas Jr., J.-K. Zhu, B. J. Staskawicz, and H. Jin
A pathogen-inducible endogenous siRNA in plant immunity
PNAS,
November 21, 2006;
103(47):
18002 - 18007.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Lu, K. Kulkarni, F. F. Souret, R. MuthuValliappan, S. S. Tej, R. S. Poethig, I. R. Henderson, S. E. Jacobsen, W. Wang, P. J. Green, et al.
MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant
Genome Res.,
October 1, 2006;
16(10):
1276 - 1288.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Xie, C. Wu, and L. Xiong
Genomic Organization, Differential Expression, and Interaction of SQUAMOSA Promoter-Binding-Like Transcription Factors and microRNA156 in Rice
Plant Physiology,
September 1, 2006;
142(1):
280 - 293.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. D. Taganov, M. P. Boldin, K.-J. Chang, and D. Baltimore
NF-{kappa}B-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses
PNAS,
August 15, 2006;
103(33):
12481 - 12486.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Mica, L. Gianfranceschi, and M. E. Pe
Characterization of five microRNA families in maize
J. Exp. Bot.,
August 1, 2006;
57(11):
2601 - 2612.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Sunkar, A. Kapoor, and J.-K. Zhu
Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance
PLANT CELL,
August 1, 2006;
18(8):
2051 - 2065.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Maggio, J.-K. Zhu, P. M. Hasegawa, and R. A. Bressan
Osmogenetics: Aristotle to Arabidopsis
PLANT CELL,
July 1, 2006;
18(7):
1542 - 1557.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Bari, B. Datt Pant, M. Stitt, and W.-R. Scheible
PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants
Plant Physiology,
July 1, 2006;
141(3):
988 - 999.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Aung, S.-I Lin, C.-C. Wu, Y.-T. Huang, C.-l. Su, and T.-J. Chiou
pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene
Plant Physiology,
July 1, 2006;
141(3):
1000 - 1011.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Navarro, P. Dunoyer, F. Jay, B. Arnold, N. Dharmasiri, M. Estelle, O. Voinnet, and J. D. G. Jones
A plant miRNA contributes to antibacterial resistance by repressing auxin signaling.
Science,
April 21, 2006;
312(5772):
436 - 439.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. R. Finkelstein
Studies of abscisic Acid perception finally flower.
PLANT CELL,
April 1, 2006;
18(4):
786 - 791.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.-J. Chiou, K. Aung, S.-I Lin, C.-C. Wu, S.-F. Chiang, and C.-l. Su
Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis
PLANT CELL,
February 1, 2006;
18(2):
412 - 421.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Yang, Y. W. Ebright, B. Yu, and X. Chen
HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2' OH of the 3' terminal nucleotide
Nucleic Acids Res.,
January 30, 2006;
34(2):
667 - 675.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. MATZKE, T. KANNO, B. HUETTEL, L. DAXINGER, and A.J.M. MATZKE
RNA-directed DNA Methylation and Pol IVb in Arabidopsis
Cold Spring Harb Symp Quant Biol,
January 1, 2006;
71(0):
449 - 459.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
B.-h. Lee, D. A. Henderson, and J.-K. Zhu
The Arabidopsis Cold-Responsive Transcriptome and Its Regulation by ICE1
PLANT CELL,
November 1, 2005;
17(11):
3155 - 3175.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Lu, S. S. Tej, S. Luo, C. D. Haudenschild, B. C. Meyers, and P. J. Green
Elucidation of the Small RNA Component of the Transcriptome
Science,
September 2, 2005;
309(5740):
1567 - 1569.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Jopling, M. Yi, A. M. Lancaster, S. M. Lemon, and P. Sarnow
Modulation of Hepatitis C Virus RNA Abundance by a Liver-Specific MicroRNA
Science,
September 2, 2005;
309(5740):
1577 - 1581.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. W. Woodward and B. Bartel
A Receptor for Auxin
PLANT CELL,
September 1, 2005;
17(9):
2425 - 2429.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Liu, P. Li, X. Li, C. Liu, S. Cao, C. Chu, and X. Cao
Loss of Function of OsDCL1 Affects MicroRNA Accumulation and Causes Developmental Defects in Rice
Plant Physiology,
September 1, 2005;
139(1):
296 - 305.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Sunkar, T. Girke, and J.-K. Zhu
Identification and characterization of endogenous small interfering RNAs from rice
Nucleic Acids Res.,
August 2, 2005;
33(14):
4443 - 4454.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Lu, Y.-H. Sun, R. Shi, C. Clark, L. Li, and V. L. Chiang
Novel and Mechanical Stress-Responsive MicroRNAs in Populus trichocarpa That Are Absent from Arabidopsis
PLANT CELL,
August 1, 2005;
17(8):
2186 - 2203.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-W. Wang, L.-J. Wang, Y.-B. Mao, W.-J. Cai, H.-W. Xue, and X.-Y. Chen
Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsis
PLANT CELL,
August 1, 2005;
17(8):
2204 - 2216.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Xie, E. Allen, N. Fahlgren, A. Calamar, S. A. Givan, and J. C. Carrington
Expression of Arabidopsis MIRNA Genes
Plant Physiology,
August 1, 2005;
138(4):
2145 - 2154.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Williams, C. C. Carles, K. S. Osmont, and J. C. Fletcher
A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes
PNAS,
July 5, 2005;
102(27):
9703 - 9708.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Zhang
miRU: an automated plant miRNA target prediction server
Nucleic Acids Res.,
July 1, 2005;
33(suppl_2):
W701 - W704.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Axtell and D. P. Bartel
Antiquity of MicroRNAs and Their Targets in Land Plants
PLANT CELL,
June 1, 2005;
17(6):
1658 - 1673.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Dong, S. T. Kim, and E. M. Lord
Plantacyanin Plays a Role in Reproduction in Arabidopsis
Plant Physiology,
June 1, 2005;
138(2):
778 - 789.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Sunkar, T. Girke, P. K. Jain, and J.-K. Zhu
Cloning and Characterization of MicroRNAs from Rice
PLANT CELL,
May 1, 2005;
17(5):
1397 - 1411.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. Mallory, D. P. Bartel, and B. Bartel
MicroRNA-Directed Regulation of Arabidopsis AUXIN RESPONSE FACTOR17 Is Essential for Proper Development and Modulates Expression of Early Auxin Response Genes
PLANT CELL,
May 1, 2005;
17(5):
1360 - 1375.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-S. Guo, Q. Xie, J.-F. Fei, and N.-H. Chua
MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development
PLANT CELL,
May 1, 2005;
17(5):
1376 - 1386.
[Abstract]
| |