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Published on November 18, 2005; 10.1104/pp.105.067884

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Received June 30, 2005
Returned for revision September 15, 2005
Accepted September 19, 2005

Induction of Thioredoxin Is Required for Nodule Development to Reduce Reactive Oxygen Species Levels in Soybean Roots

Mi-Young Lee , Ki-Hye Shin , Yun-Kyoung Kim , Ji-Yeon Suh , Young-Yun Gu , Mi-Ran Kim , Yoon-Sun Hur , Ora Son , Jin-Sun Kim , Eunsook Song , Myeong-Sok Lee , Kyoung Hee Nam , Keum Hee Hwang , Mi-Kyung Sung , Ho-Jung Kim , Jong-Yoon Chun , Miey Park , Tae-In Ahn , Choo Bong Hong , Suk-Ha Lee , Hong Jae Park , Jong-Sug Park , Desh Pal S. Verma , and Choong-Ill Cheon *

Department of Biological Science, Sookmyung Women's University, Seoul 140-742, Korea
Bio-Food and Drug Research Center, Konkuk University, Choongjoo 380-701, Korea
Department of Food and Nutrition, Sookmyung Women's University, Seoul 140-742, Korea
Seegene, Seoul 138-050, Korea
School of Biological Sciences, Seoul National University, Seoul 151-742, Korea
College of Agriculture and Life Sciences, Seoul National University, Seoul 151-742, Korea
National Institute of Agricultural Biotechnology, Rural Development Administration, Suwon 441-707, Korea
Ohio State Biotechnology Center, Ohio State University, Columbus, Ohio 43210

* Corresponding author; email: ccheon{at}sookmyung.ac.kr.

Nodules are formed on legume roots as a result of signaling between symbiotic partners and in response to the activities of numerous genes. We cloned fragments of differentially expressed genes in spot-inoculated soybean (Glycine max) roots. Many of the induced clones were similar to known genes related to oxidative stress, such as thioredoxin and {beta}-carotene hydroxylase. The deduced amino acid sequences of full-length soybean cDNAs for thioredoxin and {beta}-carotene hydroxylase were similar to those in other species. In situ RNA hybridization revealed that the thioredoxin gene is expressed on the pericycle of 2-d-old nodules and in the infected cells of mature nodules, suggesting that thioredoxin is involved in nodule development. The thioredoxin promoter was found to contain a sequence resembling an antioxidant responsive element. When a thioredoxin mutant of yeast was transformed with the soybean thioredoxin gene it became hydrogen peroxide tolerant. These observations prompted us to measure reactive oxygen species levels. These were decreased by 3- to 5-fold in 7-d-old and 27-d-old nodules, coincident with increases in the expression of thioredoxin and {beta}-carotene hydroxylase genes. Hydrogen peroxide-producing regions identified with cerium chloride were found in uninoculated roots and 2-d-old nodules, but not in 7-d-old and 27-d-old nodules. RNA interference-mediated repression of the thioredoxin gene severely impaired nodule development. These data indicate that antioxidants such as thioredoxin are essential to lower reactive oxygen species levels during nodule development.




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