Soybeans Grown in the Chernobyl Area Produce Fertile Seeds that Have Increased Heavy Metal Resistance and Modified Carbon Metabolism

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Abstract

Plants grow and reproduce in the radioactive Chernobyl area, however there has been no comprehensive characterization of these activities. Herein we report that life in this radioactive environment has led to alteration of the developing soybean seed proteome in a specific way that resulted in the production of fertile seeds with low levels of oil and β-conglycinin seed storage proteins. Soybean seeds were harvested at four, five, and six weeks after flowering, and at maturity from plants grown in either non-radioactive or radioactive plots in the Chernobyl area. The abundance of 211 proteins was determined. The results confirmed previous data indicating that alterations in the proteome include adaptation to heavy metal stress and mobilization of seed storage proteins. The results also suggest that there have been adjustments to carbon metabolism in the cytoplasm and plastids, increased activity of the tricarboxylic acid cycle, and decreased condensation of malonyl-acyl carrier protein during fatty acid biosynthesis.

Introduction

Despite the magnitude of the Chernobyl nuclear accident, local flora continues to grow and reproduce in the radio-contaminated soil. Although there has been more than 80 years of research addressing the effects of ionizing radiation on plants [1], the ongoing success of plants in the Chernobyl area was not anticipated. There have been a few molecular analyses of plants grown in the radio-contaminated Chernobyl area, and there is as yet no broad understanding of the mechanisms that underlie survival. Results from analysis of pine trees grown in the Chernobyl exclusion zone indicated genome-wide DNA damage [2], and higher nucleotide diversity in the catalase and glutathione peroxidase genes [3]. There is also DNA-hypermethylation in pine, indicating epigenetic effects in adaptation of pine to a radio-contaminated environment [4], and there appears to be a correlation between genome hypermetylation and radiation sensitivity.

In wheat plants grown in the radio-contaminated Chernobyl area for one generation, the sequences of six microsatellite loci contained complex germline mutations including loci deletion and insertions of unknown origin [5]. In later generations, the wheat DNA showed gains and losses of repeat-DNA and the complete loss of microsatellite bands associated with 13 single-copy monomorphic loci [6]. The progeny of Arabidopsis thaliana plants collected from radio-contaminated area around the Chernobyl nuclear power plant were resistant to high concentrations of the mutagens Rose Bengal and methyl methane sulfonate [7]. Additionally, these plants showed significant differences in expression of radical-scavenging and DNA-repair genes upon exposure to mutagens, and a 10-fold lower frequency of extrachromosomal homologous recombination [7]. Analysis of possible molecular mechanisms involved in such resistance revealed a high level of global genome methylation [7].

To complement these genomics and mutagenic studies with proteomics data is the next step in understanding adaptation to permanently increased levels of ionizing radiation. Recently, we analyzed protein abundance in mature seeds harvested from first generation soybean plants grown in radioactive and non-radioactive plots in the Chernobyl area [8]. We found evidence suggesting adaptation to heavy metal stress, protection against radiation damage, and mobilization of seed storage proteins are involved in plant adjustments to increased levels of ionizing radiation [8]. We now extend these data by reporting herein a comparison of changes in protein abundance during seed development of second generation plants grown in either non-radioactive or radioactive plots in the Chernobyl area.

Citation: Klubicová K, Danchenko M, Skultety L, Berezhna VV, Uvackova L, et al.  (2012) Soybeans Grown in the Chernobyl Area Produce Fertile Seeds that Have Increased Heavy Metal Resistance and Modified Carbon Metabolism. PLoS ONE 7(10):          e48169.            doi:10.1371/journal.pone.0048169

Editor: Joshua L. Heazlewood,         Lawrence Berkeley National Laboratory, United States of America

 

Received: May 24, 2012; Accepted: September 21, 2012; Published: October 26, 2012

Copyright: © 2012 Klubicová et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This research was supported by the Seventh Framework Program of the European Union – International Reintegration Grant (MIRG-CT-2007-200165), Scientific Grant Agency of the Ministry of Education of the Slovak Republic and the Academy of Sciences (VEGA-2/0126/11), the Slovak Research and Development Agency (APVV-0740-11), and Research & Development Operational Program funded by the ERDF – Centre of Excellence for White-Green Biotechnology (ITMS 26220120054). MD was supported by the National Scholarship Program of the Slovak Republic. This paper reflects only the author’s views and the Community is not liable for any use that might be made of information contained herein.

Competing interests: The authors have declared that no competing interests exist.

* E-mail: hajduch@savba.sk

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0048169

http://www.chernobylproteomics.sav.sk/home

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