Plant Physiology Preview Published on February 27, 2003; 10.1104/pp.013623
Received August 28, 2002
Returned for revision September 9, 2002
Accepted November 18, 2002
Auxin Signaling in Arabidopsis Leaf Vascular Development
Jim Mattsson , Wenzislava Ckurshumova , and Thomas Berleth *
Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, Canada M5S 3B2
* Corresponding author; email: berleth{at}botany.utoronto.ca.
A number of observations have implicated auxin in the formation of vascular tissues in plant organs. These include vascular strand formation in response to local auxin application, the effects of impaired auxin transport on vascular patterns and suggestive phenotypes of Arabidopsis auxin response mutants. In this study, we have used molecular markers to visualize auxin response patterns in developing Arabidopsis leaves as well as Arabidopsis mutants and transgenic plants to trace pathways of auxin signal transduction controlling the expression of early procambial genes. We show that in young Arabidopsis leaf primordia, molecular auxin response patterns presage sites of procambial differentiation. This is the case not only in normal development but also upon experimental manipulation of auxin transport suggesting that local auxin signals are instrumental in patterning Arabidopsis leaf vasculature. We further found that the activity of the Arabidopsis gene MONOPTEROS, which is required for proper vascular differentiation, is also essential in a spectrum of auxin responses, which include the regulation of rapidly auxin-inducible AUX/IAA genes, and discovered the tissue-specific vascular expression profile of the class I homeodomain-leucine zipper gene, AtHB20. Interestingly, MONOPTEROS activity is a limiting factor in the expression of AtHB8 and AtHB20, two genes encoding transcriptional regulators expressed early in procambial development. Our observations connect general auxin signaling with early controls of vascular differentiation and suggest molecular mechanisms for auxin signaling in patterned cell differentiation.
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|
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|
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|

|
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|
 |
|

|
 |

|
 |
 
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324(5935):
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|
 |
|

|
 |

|
 |
 
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60(4):
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[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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|
 |
|

|
 |

|
 |
 
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|
 |
|

|
 |

|
 |
 
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|
 |
|

|
 |

|
 |
 
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|
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|
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|
 |
|

|
 |

|
 |
 
F. Bai and D. A. DeMason
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|
 |
|

|
 |

|
 |
 
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58(13):
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|
 |
|

|
 |

|
 |
 
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(2007)
erm180v1.
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|
 |
|

|
 |

|
 |
 
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September 1, 2007;
19(9):
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|
 |
|

|
 |

|
 |
 
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AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis
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134(14):
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[Full Text]
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|
 |
|

|
 |

|
 |
 
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Components of the Arabidopsis mRNA Decapping Complex Are Required for Early Seedling Development
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|
 |
|

|
 |

|
 |
 
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144(1):
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Muto, M. K. Watahiki, D. Nakamoto, M. Kinjo, and K. T. Yamamoto
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May 1, 2007;
144(1):
187 - 196.
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|
 |
|

|
 |

|
 |
 
E. Costantini, L. Landi, O. Silvestroni, T. Pandolfini, A. Spena, and B. Mezzetti
Auxin Synthesis-Encoding Transgene Enhances Grape Fecundity
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143(4):
1689 - 1694.
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|
 |
|

|
 |

|
 |
 
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|
 |
|

|
 |

|
 |
 
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October 1, 2006;
133(19):
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[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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20(13):
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|
 |
|

|
 |

|
 |
 
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PLANT CELL,
June 1, 2006;
18(6):
1396 - 1411.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. K. Floyd, C. S. Zalewski, and J. L. Bowman
Evolution of Class III Homeodomain-Leucine Zipper Genes in Streptophytes
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May 1, 2006;
173(1):
373 - 388.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Cnops, P. Neyt, J. Raes, M. Petrarulo, H. Nelissen, N. Malenica, C. Luschnig, O. Tietz, F. Ditengou, K. Palme, et al.
The TORNADO1 and TORNADO2 Genes Function in Several Patterning Processes during Early Leaf Development in Arabidopsis thaliana
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April 1, 2006;
18(4):
852 - 866.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. S. Smith, S. Guyomarc'h, T. Mandel, D. Reinhardt, C. Kuhlemeier, and P. Prusinkiewicz
A plausible model of phyllotaxis
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January 31, 2006;
103(5):
1301 - 1306.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Yoshida, H. Kuriyama, and H. Fukuda
Inhibition of Transdifferentiation into Tracheary Elements by Polar Auxin Transport Inhibitors Through Intracellular Auxin Depletion
Plant Cell Physiol.,
December 1, 2005;
46(12):
2019 - 2028.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Pekker, J. P. Alvarez, and Y. Eshed
Auxin Response Factors Mediate Arabidopsis Organ Asymmetry via Modulation of KANADI Activity
PLANT CELL,
November 1, 2005;
17(11):
2899 - 2910.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Nishimura, T. Wada, K. T. Yamamoto, and K. Okada
The Arabidopsis STV1 Protein, Responsible for Translation Reinitiation, Is Required for Auxin-Mediated Gynoecium Patterning
PLANT CELL,
November 1, 2005;
17(11):
2940 - 2953.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-L. Xiao, S. R. Smith, N. Ishmael, J. C. Redman, N. Kumar, E. L. Monaghan, M. Ayele, B. J. Haas, H. C. Wu, and C. D. Town
Analysis of the cDNAs of Hypothetical Genes on Arabidopsis Chromosome 2 Reveals Numerous Transcript Variants
Plant Physiology,
November 1, 2005;
139(3):
1323 - 1337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Vieten, S. Vanneste, J. Wisniewska, E. Benkova, R. Benjamins, T. Beeckman, C. Luschnig, and J. Friml
Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression
Development,
October 15, 2005;
132(20):
4521 - 4531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Wang, B. Jones, Z. Li, P. Frasse, C. Delalande, F. Regad, S. Chaabouni, A. Latche, J.-C. Pech, and M. Bouzayen
The Tomato Aux/IAA Transcription Factor IAA9 Is Involved in Fruit Development and Leaf Morphogenesis
PLANT CELL,
October 1, 2005;
17(10):
2676 - 2692.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. I.A. Calderon-Villalobos, C. Kuhnle, E. M.N. Dohmann, H. Li, M. Bevan, and C. Schwechheimer
The Evolutionarily Conserved TOUGH Protein Is Required for Proper Development of Arabidopsis thaliana
PLANT CELL,
September 1, 2005;
17(9):
2473 - 2485.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Wang, S. B. Tiwari, G. Hagen, and T. J. Guilfoyle
AUXIN RESPONSE FACTOR7 Restores the Expression of Auxin-Responsive Genes in Mutant Arabidopsis Leaf Mesophyll Protoplasts
PLANT CELL,
July 1, 2005;
17(7):
1979 - 1993.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. W. WOODWARD and B. BARTEL
Auxin: Regulation, Action, and Interaction
Ann. Bot.,
April 1, 2005;
95(5):
707 - 735.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Koizumi, S. Naramoto, S. Sawa, N. Yahara, T. Ueda, A. Nakano, M. Sugiyama, and H. Fukuda
VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation
Development,
April 1, 2005;
132(7):
1699 - 1711.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Prigge, D. Otsuga, J. M. Alonso, J. R. Ecker, G. N. Drews, and S. E. Clark
Class III Homeodomain-Leucine Zipper Gene Family Members Have Overlapping, Antagonistic, and Distinct Roles in Arabidopsis Development
PLANT CELL,
January 1, 2005;
17(1):
61 - 76.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Zgurski, R. Sharma, D. A. Bolokoski, and E. A. Schultz
Asymmetric Auxin Response Precedes Asymmetric Growth and Differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis Leaves
PLANT CELL,
January 1, 2005;
17(1):
77 - 91.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Friml, X. Yang, M. Michniewicz, D. Weijers, A. Quint, O. Tietz, R. Benjamins, P. B. F. Ouwerkerk, K. Ljung, G. Sandberg, et al.
A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux
Science,
October 29, 2004;
306(5697):
862 - 865.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Navarro, N. Efremova, J. F. Golz, R. Rubiera, M. Kuckenberg, R. Castillo, O. Tietz, H. Saedler, and Z. Schwarz-Sommer
Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development
Development,
August 1, 2004;
131(15):
3649 - 3659.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Scarpella, P. Francis, and T. Berleth
Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation
Development,
July 15, 2004;
131(14):
3445 - 3455.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. M. Carland and T. Nelson
COTYLEDON VASCULAR PATTERN2-Mediated Inositol (1,4,5) Triphosphate Signal Transduction Is Essential for Closed Venation Patterns of Arabidopsis Foliar Organs
PLANT CELL,
May 1, 2004;
16(5):
1263 - 1275.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Zhong and Z.-H. Ye
amphivasal vascular bundle 1, a Gain-of-Function Mutation of the IFL1/REV Gene, Is Associated with Alterations in the Polarity of Leaves, Stems and Carpels
Plant Cell Physiol.,
April 15, 2004;
45(4):
369 - 385.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. S. Hardtke, W. Ckurshumova, D. P. Vidaurre, S. A. Singh, G. Stamatiou, S. B. Tiwari, G. Hagen, T. J. Guilfoyle, and T. Berleth
Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4
Development,
March 1, 2004;
131(5):
1089 - 1100.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. P. Keller, R. Stahlberg, L. S. Barkawi, and J. D. Cohen
Long-Term Inhibition by Auxin of Leaf Blade Expansion in Bean and Arabidopsis
Plant Physiology,
March 1, 2004;
134(3):
1217 - 1226.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Tatematsu, S. Kumagai, H. Muto, A. Sato, M. K. Watahiki, R. M. Harper, E. Liscum, and K. T. Yamamoto
MASSUGU2 Encodes Aux/IAA19, an Auxin-Regulated Protein That Functions Together with the Transcriptional Activator NPH4/ARF7 to Regulate Differential Growth Responses of Hypocotyl and Formation of Lateral Roots in Arabidopsis thaliana
PLANT CELL,
February 1, 2004;
16(2):
379 - 393.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. K. Deyholos, G. F. Cavaness, B. Hall, E. King, J. Punwani, J. Van Norman, and L. E. Sieburth
VARICOSE, a WD-domain protein, is required for leaf blade development
Development,
December 29, 2003;
130(26):
6577 - 6588.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ohashi-Ito and H. Fukuda
HD-Zip III Homeobox Genes that Include a Novel Member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are Involved in Procambium and Xylem Cell Differentiation
Plant Cell Physiol.,
December 15, 2003;
44(12):
1350 - 1358.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q. J. Steynen and E. A. Schultz
The FORKED genes are essential for distal vein meeting in Arabidopsis
Development,
October 1, 2003;
130(19):
4695 - 4708.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|