Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.)

Abstract 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 detoxific...

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Main Authors: Weixuan Cong, Yiling Miao, Lei Xu, Yunhong Zhang, Chunlei Yuan, Junmeng Wang, Tingting Zhuang, Xiuyun Lin, Lili Jiang, Ningning Wang, Jian Ma, Karen A. Sanguinet, Bao Liu, Sachin Rustgi, Xiufang Ou
Format: Article
Language:English
Published: BMC 2019-06-01
Series:BMC Plant Biology
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Online Access:http://link.springer.com/article/10.1186/s12870-019-1887-7
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spelling doaj-c295d867d15f463e8fc6bfd4feda3c332020-11-25T03:46:23ZengBMCBMC Plant Biology1471-22292019-06-0119111410.1186/s12870-019-1887-7Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.)Weixuan Cong0Yiling Miao1Lei Xu2Yunhong Zhang3Chunlei Yuan4Junmeng Wang5Tingting Zhuang6Xiuyun Lin7Lili Jiang8Ningning Wang9Jian Ma10Karen A. Sanguinet11Bao Liu12Sachin Rustgi13Xiufang Ou14Key Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityJilin Academy of Agricultural SciencesKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityJilin Agriculture UniversityJilin Agriculture UniversityDepartment of Crop and Soil Sciences, Washington State UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityDepartment of Crop and Soil Sciences, Washington State UniversityKey Laboratory of Molecular Epigenetics of MOE and Institute of Genetics & Cytology, Northeast Normal UniversityAbstract 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 P1B 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.http://link.springer.com/article/10.1186/s12870-019-1887-7Heavy metal stressTransgenerational memoryGene expressionDNA methylation
collection DOAJ
language English
format Article
sources DOAJ
author Weixuan Cong
Yiling Miao
Lei Xu
Yunhong Zhang
Chunlei Yuan
Junmeng Wang
Tingting Zhuang
Xiuyun Lin
Lili Jiang
Ningning Wang
Jian Ma
Karen A. Sanguinet
Bao Liu
Sachin Rustgi
Xiufang Ou
spellingShingle Weixuan Cong
Yiling Miao
Lei Xu
Yunhong Zhang
Chunlei Yuan
Junmeng Wang
Tingting Zhuang
Xiuyun Lin
Lili Jiang
Ningning Wang
Jian Ma
Karen A. Sanguinet
Bao Liu
Sachin Rustgi
Xiufang Ou
Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.)
BMC Plant Biology
Heavy metal stress
Transgenerational memory
Gene expression
DNA methylation
author_facet Weixuan Cong
Yiling Miao
Lei Xu
Yunhong Zhang
Chunlei Yuan
Junmeng Wang
Tingting Zhuang
Xiuyun Lin
Lili Jiang
Ningning Wang
Jian Ma
Karen A. Sanguinet
Bao Liu
Sachin Rustgi
Xiufang Ou
author_sort Weixuan Cong
title 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_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_sort transgenerational memory of gene expression changes induced by heavy metal stress in rice (oryza sativa l.)
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2019-06-01
description Abstract 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 P1B 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.
topic Heavy metal stress
Transgenerational memory
Gene expression
DNA methylation
url http://link.springer.com/article/10.1186/s12870-019-1887-7
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