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Diurnal regulation of alternative splicing associated with thermotolerance in rice by two glycine-rich RNA-binding proteins

Rice (Oryza sativa L.) production is threatened by global warming associated with extreme high temperatures, and rice heat sensitivity is differed when stress occurs between daytime and nighttime. However, the underlying molecular mechanism are largely unknown. We show here that two glycine-rich RNA binding proteins, OsGRP3 and OsGRP162, are required for thermotolerance in rice, especially at nighttime. The rhythmic expression of OsGRP3/OsGRP162 peaks at midnight, and at these coincident times, is increased by heat stress. This is largely dependent on the evening complex component OsELF3-2.

Chuang Yang, Anni Luo, Hai-Ping Lu, Seth Jon Davis, Jian-Xiang Liu

Sci Bull (Beijing); 2024 Jan 15; 69(1):59-71. doi: 10.1016/j.scib.2023.11.046. 

Abstract

Rice (Oryza sativa L.) production is threatened by global warming associated with extreme high temperatures, and rice heat sensitivity is differed when stress occurs between daytime and nighttime. However, the underlying molecular mechanism are largely unknown. We show here that two glycine-rich RNA binding proteins, OsGRP3 and OsGRP162, are required for thermotolerance in rice, especially at nighttime. The rhythmic expression of OsGRP3/OsGRP162 peaks at midnight, and at these coincident times, is increased by heat stress. This is largely dependent on the evening complex component OsELF3-2. We next found that the double mutant of OsGRP3/OsGRP162 is strikingly more sensitive to heat stress in terms of survival rate and seed setting rate when comparing to the wild-type plants. Interestingly, the defect in thermotolerance is more evident when heat stress occurred in nighttime than that in daytime. Upon heat stress, the double mutant of OsGRP3/OsGRP162 displays globally reduced expression of heat-stress responsive genes, and increases of mRNA alternative splicing dominated by exon-skipping. This study thus reveals the important role of OsGRP3/OsGRP162 in thermotolerance in rice, and unravels the mechanism on how OsGRP3/OsGRP162 regulate thermotolerance in a diurnal manner.

 

See https://pubmed.ncbi.nlm.nih.gov/38044192/

 

Figure 7: Working models for the function of OsGRP3 and OsGRP162 in diurnal thermotolerance. (a) Diurnal expression of OsGRP3/OsGRP162 regulated by OsELF3-2. Under warm day conditions, the expression of OsGRP3/OsGRP162 (blue line) is largely suppressed by EC at midnight because OsELF3-2 (red line) is highly expressed at this timepoint. Under warm night conditions, the expression of OsELF3-2 is down-regulated by heat stress, lifting the expression level of OsGRP3/OsGRP162 at midnight. (b) Promoting exon inclusion by OsGRP3/OsGRP162 under heat stress conditions. Serine-rich (SR) proteins bind to exonic splicing enhancers (ESEs) and interact with U1/U2 components to stimulate RNA splicing and joining two adjacent exons, in contrast, glycine-rich (GR) proteins OsGRP3/OsGRP162 bind to ESEs and interact with U1/U2 components to promote exon inclusion (prevent exon skipping) in rice under heat stress conditions. (c) Diurnal regulation of thermotolerance by OsGRP3/OsGRP162. Heat stress rhythmically down-regulates the expression of OsELF3, one of the EC components, to release the inhibitory effect of EC on the expression of OsGRP3/OsGRP162, leading to rhythmical expression peak of OsGRP3/OsGRP162 at midnight (ZT 18 h) and diurnal thermotolerance in rice.

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