Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis

doi:10.1104/pp.002857

Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis

Yong Hwa Cheong , Hur-Song Chang , Rajeev Gupta , Xun Wang , Tong Zhu ^*, and Sheng Luan

Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (Y.H.C., R.G., S.L.); and Torrey Mesa Research Institute, Syngenta Research and Technology, San Diego, California 92121 (H.-S.C., X.W., T.Z.)

^* Corresponding author; email: tong.zhu{at}syngenta.com.

Mechanical wounding not only damages plant tissues, but also provides pathways for pathogen invasion. To understand plant responses to wounding at a genomic level, we have surveyed the transcriptional response of 8,200 genes in Arabidopsis plants. Approximately 8% of these genes were altered by wounding at steady-state mRNA levels. Studies of expression patterns of these genes provide new information on the interactions between wounding and other signals, including pathogen attack, abiotic stress factors, and plant hormones. For example, a number of wound-responsive genes encode proteins involved in pathogen response. These include signaling molecules for the pathogen resistance pathway and enzymes required for cell wall modification and secondary metabolism. Many osmotic stress- and heat shock-regulated genes were highly responsive to wounding. Although a number of genes involved in ethylene, jasmonic acid, and abscisic acid pathways were activated, many in auxin responses were suppressed by wounding. These results further dissected the nature of mechanical wounding as a stress signal and identified new genes that may play a role in wounding and other signal transduction pathways.

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[Abstract] [Full Text] [PDF]

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PLANT CELL, November 1, 2003; 15(11): 2551 - 2565.
[Abstract] [Full Text] [PDF]

C. Johnson, E. Boden, and J. Arias
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PLANT CELL, August 1, 2003; 15(8): 1846 - 1858.
[Abstract] [Full Text] [PDF]

J. E. Dombrowski
Salt Stress Activation of Wound-Related Genes in Tomato Plants
Plant Physiology, August 1, 2003; 132(4): 2098 - 2107.
[Abstract] [Full Text] [PDF]

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PNAS, July 8, 2003; 100(14): 8595 - 8600.
[Abstract] [Full Text] [PDF]

K.-i. Hayashi, A. M. Jones, K. Ogino, A. Yamazoe, Y. Oono, M. Inoguchi, H. Kondo, and H. Nozaki
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J. Biol. Chem., June 20, 2003; 278(26): 23797 - 23806.
[Abstract] [Full Text] [PDF]

R. L. Brown, K. Kazan, K. C. McGrath, D. J. Maclean, and J. M. Manners
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Plant Physiology, June 1, 2003; 132(2): 1020 - 1032.
[Abstract] [Full Text] [PDF]

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J. Biol. Chem., May 23, 2003; 278(21): 18945 - 18952.
[Abstract] [Full Text] [PDF]

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