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 detoxification, transport and/or sequestration. The P 1B subfamily of the H eavy M etal-transporting P-type A TPases (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.

Epigenetic regulation in plant abiotic stress responses

“…In addition to the memory during priming, increasing evidence indicates that DNA sequence‐independent epigenetic modification could transmit from one generation to the next generation (Lang‐Mladek et al 2010; Iwasaki and Paszkowski 2014; Zheng et al 2017; Cong et al 2019), which is referred to as “transgenerational memory” (Heard and Martienssen 2014). The formation of stress‐induced transgenerational memory in the progeny benefit plants to achieve a better balance between survival and reproduction (Molinier et al 2006).…”

“…Thus, one possibility is that the maintenance of drought‐induced DNA methylation status in progeny participates in the drought stress response and in the long‐term adaptation to drought stress conditions (Zheng et al 2017). More recently, another study indicated that DNA methylation participates in the transgenerational memory of the response to heavy metal stress in rice (Cong et al 2019). Cong et al demonstrated that Heavy Metal‐transporting P‐type ATPase genes (HMAs) was upregulated in response to heavy metal stress and the transgenerational memory of gene expression was observed after the removal of heavy metals (Cong et al 2019).…”

“…More recently, another study indicated that DNA methylation participates in the transgenerational memory of the response to heavy metal stress in rice (Cong et al 2019). Cong et al demonstrated that Heavy Metal‐transporting P‐type ATPase genes (HMAs) was upregulated in response to heavy metal stress and the transgenerational memory of gene expression was observed after the removal of heavy metals (Cong et al 2019). They further revealed that the DNA methylation status of a Tos17 retrotransposon was altered in response to the heavy metal stress and the altered DNA methylation displayed transgenerational inheritance within three generations.…”

Epigenetic Mechanisms of Plant Adaptation to Biotic and Abiotic Stresses

“…Multiple cases of such transgenerationally inheritable epigenetic changes (epimutations), both naturally arisen and artificially induced, were described [ 26 ]. The formation of stress-induced transgenerational memory obviously should benefit the plant progeny to achieve a better stress resistance [ 87 , 88 ].…”

“…Whether the frequently occurring heavy metal-contamination of soil should be regarded as environmental stress that has transgenerationally inheritable effects on DNA methylation was studied in rice [ 88 , 97 ]. Treatment of 10-day old rice seedlings with the heavy metals, Cu 2+ , Cd 2+ , Cr 3+ , and Hg 2+ , significantly inhibited shoot and root development and changed DNA methylation patterns in four of the six TEs and 11 of the 12 protein-encoding genes that were analyzed [ 97 ].…”