Cytosine methylations in the promoter regions of genes involved in the cellular oxidation equilibrium pathways affect rice heat tolerance

Abstract

Background: High temperatures, particularly at night, decrease rice yield and quality. As high nighttime temperatures (HNTs) become increasingly frequent due to climate change, it is imperative to develop rice crops that tolerate HNTs. DNA methylation may represent a potential avenue for HNT-tolerant rice strain development, as this mechanism regulates gene activity and cellular phenotype in response to adverse environmental conditions without changing the nucleotide sequence. Results: After HNT exposure, the methylation patterns of cytosines in the CHH context differed noticeably between two coisogenic rice strains with significantly different levels in heat tolerance. Methylation differences between strains were primarily observed on successive cytosines in the promoter or downstream regions of transcription factors and transposon elements. In contrast to the heat-sensitive rice strain, the regions 358-359 bp and 2-60 bp downstream of two basal transcriptional factors (TFIID subunit 11 and mediator of RNA polymerase II transcription subunit 31, respectively) were fully demethylated in the heat-tolerant strain after HNT exposure. In the heat-tolerant strain, HNTs reversed the methylation patterns of successive cytosines in the promoter regions of various genes involved in abscisic acid (ABA)-related reactive oxygen species (ROS) equilibrium pathways, including the pentatricopeptide repeat domain gene PPR (LOC_Os07g28900) and the homeobox domain gene homeobox (LOC_ Os01g19694). Indeed, PRR expression was inhibited in heat-sensitive rice strains, and the methylation rates of the cytosines in the promoter region of PRR were greater in heat-sensitive strains as compared to heat-tolerant strains. Conclusions: After HNT exposure, cytosines in the CHH context were more likely than cytosines in other contexts to be methylated differently between the heat-sensitive and heat-tolerant rice strains. Methylation in the promoter regions of the genes associated with ABA-related oxidation and ROS scavenging improved heat tolerance in rice. Our results help to clarify the molecular mechanisms underlying rice heat tolerance.

DNA methylation-mediated ROS production contributes to seed abortion in litchi

“…Mutations in MSD , such as the oiwa mutant, disrupt ROS homeostasis, resulting in high ROS levels in the embryo sac and leading to sterility or arrested embryogenesis (Victoria Martin et al 2013 ). Recently, there have been reports highlighting the crucial roles of DNA methylation-mediated ROS homeostasis in various aspects of plant development and stress response, including salt stress (Chen et al 2015 ; Hu et al 2021 ), heat stress(Ma et al 2018 ; Sakai et al 2022 ; Zhu et al 2021 ), chilling/freezing stress(Guo et al 2019 ; Zheng et al 2022 ), and fruit ripening (He et al 2020 ). For instance, the application of 5-azaC, an inhibitor of DNA methyltransferase, has been found to enhance the rates of superoxide anion (O 2 − ) production, thereby contributing to the ripening of berry fruits (Guo et al 2019 ).…”

Systematic identification and characterization of microRNAs with target genes involved in high night temperature stress at the filling stage of rice

“…Two coisogenic rice strains, heat‐sensitive line XN0437S and heat‐tolerant line XN0437T, were previously isolated in our laboratory (Liao et al, 2011), showing stable and repeatable heat tolerance differences under high night temperature stress at the filling stage (He et al, 2020; Lei et al, 2018; Zhang et al, 2017). This study also investigated agronomic traits of the heat‐sensitive and heat‐tolerant lines at the maturity stage (Figure 1).…”

“…In this study, the heat‐sensitive line XN0437S and heat‐tolerant line XN0437T of rice near‐isogenic lines with significant differences in heat tolerance at the filling stage were used as materials. The genomes of these two lines showed only 1.8% polymorphism when 887 simple sequence repeat markers were used to screen their genomic DNA (He et al, 2020; Lei et al, 2018; Liao et al, 2011; Zhang et al, 2017). However, after high night temperature stress, there were significant differences in grain weight between these two lines (He et al, 2020; Lei et al, 2018; Zhang et al, 2017).…”

“…The genomes of these two lines showed only 1.8% polymorphism when 887 simple sequence repeat markers were used to screen their genomic DNA (He et al, 2020; Lei et al, 2018; Liao et al, 2011; Zhang et al, 2017). However, after high night temperature stress, there were significant differences in grain weight between these two lines (He et al, 2020; Lei et al, 2018; Zhang et al, 2017).…”

An Epigenetic Alphabet of Crop Adaptation to Climate Change

“…Regarding heat stress, CHH methylation patterns differed between two rice lines showing different levels of heat tolerance ( He et al, 2020 ). In barley ( Hordeum vulgare L.), increasing air temperature by 3°C led to increased levels and altering DNA methylation patterns while in cotton ( Gossypium hirsutum L.) prolonged heat stress led to methylation changes in the promoter of anther-expressed genes.…”