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Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.)
BACKGROUND: Heavy metal toxicity has become a major threat to sustainable crop production worldwide. Thus, considerable interest has been placed on deciphering the mechanisms that allow plants to combat heavy metal stress. Strategies to deal with heavy metals are largely focused on detoxification, t...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598230/ https://www.ncbi.nlm.nih.gov/pubmed/31248374 http://dx.doi.org/10.1186/s12870-019-1887-7 |
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author | Cong, Weixuan Miao, Yiling Xu, Lei Zhang, Yunhong Yuan, Chunlei Wang, Junmeng Zhuang, Tingting Lin, Xiuyun Jiang, Lili Wang, Ningning Ma, Jian Sanguinet, Karen A. Liu, Bao Rustgi, Sachin Ou, Xiufang |
author_facet | Cong, Weixuan Miao, Yiling Xu, Lei Zhang, Yunhong Yuan, Chunlei Wang, Junmeng Zhuang, Tingting Lin, Xiuyun Jiang, Lili Wang, Ningning Ma, Jian Sanguinet, Karen A. Liu, Bao Rustgi, Sachin Ou, Xiufang |
author_sort | Cong, Weixuan |
collection | PubMed |
description | BACKGROUND: Heavy metal toxicity has become a major threat to sustainable crop production worldwide. Thus, considerable interest has been placed on deciphering the mechanisms that allow plants to combat heavy metal stress. Strategies to deal with heavy metals are largely focused on detoxification, transport and/or sequestration. The P(1B) subfamily of the Heavy Metal-transporting P-type ATPases (HMAs) was shown to play a crucial role in the uptake and translocation of heavy metals in plants. Here, we report the locus-specific expression changes in the rice HMA genes together with several low-copy cellular genes and transposable elements upon the heavy metal treatment and monitored the transgenerational inheritance of the altered expression states. We reveal that plants cope with heavy metal stress by making heritable changes in gene expression and further determined gene-specific responses to heavy metal stress. RESULTS: We found most HMA genes were upregulated in response to heavy metal stress, and furthermore found evidence of transgenerational memory via changes in gene regulation even after the removal of heavy metals. To explore whether DNA methylation was also altered in response to the heavy metal stress, we selected a Tos17 retrotransposon for bisulfite sequencing and studied its methylation state across three generations. We found the DNA methylation state of Tos17 was altered in response to the heavy metal stress and showed transgenerational inheritance. CONCLUSIONS: Collectively, the present study elucidates heritable changes in gene expression and DNA methylation in rice upon exposure to heavy metal stress and discusses implications of this knowledge in breeding for heavy metal tolerant crops. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1887-7) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6598230 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-65982302019-07-11 Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) Cong, Weixuan Miao, Yiling Xu, Lei Zhang, Yunhong Yuan, Chunlei Wang, Junmeng Zhuang, Tingting Lin, Xiuyun Jiang, Lili Wang, Ningning Ma, Jian Sanguinet, Karen A. Liu, Bao Rustgi, Sachin Ou, Xiufang BMC Plant Biol Research Article BACKGROUND: Heavy metal toxicity has become a major threat to sustainable crop production worldwide. Thus, considerable interest has been placed on deciphering the mechanisms that allow plants to combat heavy metal stress. Strategies to deal with heavy metals are largely focused on detoxification, transport and/or sequestration. The P(1B) subfamily of the Heavy Metal-transporting P-type ATPases (HMAs) was shown to play a crucial role in the uptake and translocation of heavy metals in plants. Here, we report the locus-specific expression changes in the rice HMA genes together with several low-copy cellular genes and transposable elements upon the heavy metal treatment and monitored the transgenerational inheritance of the altered expression states. We reveal that plants cope with heavy metal stress by making heritable changes in gene expression and further determined gene-specific responses to heavy metal stress. RESULTS: We found most HMA genes were upregulated in response to heavy metal stress, and furthermore found evidence of transgenerational memory via changes in gene regulation even after the removal of heavy metals. To explore whether DNA methylation was also altered in response to the heavy metal stress, we selected a Tos17 retrotransposon for bisulfite sequencing and studied its methylation state across three generations. We found the DNA methylation state of Tos17 was altered in response to the heavy metal stress and showed transgenerational inheritance. CONCLUSIONS: Collectively, the present study elucidates heritable changes in gene expression and DNA methylation in rice upon exposure to heavy metal stress and discusses implications of this knowledge in breeding for heavy metal tolerant crops. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1887-7) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-27 /pmc/articles/PMC6598230/ /pubmed/31248374 http://dx.doi.org/10.1186/s12870-019-1887-7 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Cong, Weixuan Miao, Yiling Xu, Lei Zhang, Yunhong Yuan, Chunlei Wang, Junmeng Zhuang, Tingting Lin, Xiuyun Jiang, Lili Wang, Ningning Ma, Jian Sanguinet, Karen A. Liu, Bao Rustgi, Sachin Ou, Xiufang Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) |
title | Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) |
title_full | Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) |
title_fullStr | Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) |
title_full_unstemmed | Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) |
title_short | Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) |
title_sort | transgenerational memory of gene expression changes induced by heavy metal stress in rice (oryza sativa l.) |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598230/ https://www.ncbi.nlm.nih.gov/pubmed/31248374 http://dx.doi.org/10.1186/s12870-019-1887-7 |
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