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

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.

Chao HeHong-Yu ZhangYong-Xin ZhangPei FuLi-Li YouWen-Bo XiaoZhao-Hai WangHai-Yan SongYing-Jin HuangJiang-Lin Liao

BMC Genomics; 2020 Aug 14;21(1):560.  doi: 10.1186/s12864-020-06975-3.

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.

 

See: https://pubmed.ncbi.nlm.nih.gov/32799794/

 

Figure 6: The DNA sequence, methylation ratio, expression patterns of gene PPR in six rice germplasms. (a) The nucleotide sequence 1495–1577 bp upstream from the TSS of gene PPR in the typical heat-sensitive (Labelle, Kashihikari and OM997) and heat-tolerant (Huazhan, Qiyinzhan and Simiao) rice germplasms. (b) The methylation rates of the cytosines 1495–1577 bp upstream of gene PPR in the heat-sensitive and heat-tolerant rice germplasms under high nighttime temperature and normal temperature conditions. (c) The gene expression patterns of PPR in the typical heat-sensitive and heat-tolerant rice germplasms under high nighttime temperature and normal temperature conditions (original full length gel images are presented in Additional file 2: Figure S4–S9); the rice Actin1 (LOC_Os03g50885) gene was used as an internal control. T1, T2, and T3 indicate replicates exposed to high nighttime temperatures; CK1, CK2, and CK3 indicate control replicates kept at normal temperatures. (d) Weights of the rice grains produced by heat-sensitive and heat-tolerant germplasms exposed to either high nighttime temperatures or normal temperatures

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