RNA structure mediated thermoregulation: What can we learn from plants?

Thomas, S.E.; Balcerowicz, Martin; Chung, Betty Y.-W.

doi:10.3389/fpls.2022.938570

Cited by 17 publications

(11 citation statements)

References 66 publications

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“…At elevated temperatures, the translation of PHYTOCHROME-INTERACTING FACTOR 7 ( PIF7 ), HEAT SHOCK FACTOR A2 ( HSFA2 ) and WRKY22 was enhanced. The expression levels of these transcription factors control plant thermomorphogenesis, heat acclimation and other stress responses ( 76 , 77 ). The discovery of RNA thermometers in photosynthetic eukaryotes opens up new research directions in thermoregulation and new biotechnological applications in plants and algae.…”

Section: Discussionmentioning

confidence: 99%

An RNA thermometer in the chloroplast genome of Chlamydomonas facilitates temperature-controlled gene expression

Chung,

Loiacono,

Neupert

et al. 2023

Nucleic Acids Research

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Riboregulators such as riboswitches and RNA thermometers provide simple, protein-independent tools to control gene expression at the post-transcriptional level. In bacteria, RNA thermometers regulate protein synthesis in response to temperature shifts. Thermometers outside of the bacterial world are rare, and in organellar genomes, no RNA thermometers have been identified to date. Here we report the discovery of an RNA thermometer in a chloroplast gene of the unicellular green alga Chlamydomonas reinhardtii. The thermometer, residing in the 5′ untranslated region of the psaA messenger RNA forms a hairpin-type secondary structure that masks the Shine–Dalgarno sequence at 25°C. At 40°C, melting of the secondary structure increases accessibility of the Shine–Dalgarno sequence to initiating ribosomes, thus enhancing protein synthesis. By targeted nucleotide substitutions and transfer of the thermometer into Escherichia coli, we show that the secondary structure is necessary and sufficient to confer the thermometer properties. We also demonstrate that the thermometer provides a valuable tool for inducible transgene expression from the Chlamydomonas plastid genome, in that a simple temperature shift of the algal culture can greatly increase recombinant protein yields.

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Section: Discussionmentioning

confidence: 99%

An RNA thermometer in the chloroplast genome of Chlamydomonas facilitates temperature-controlled gene expression

Chung,

Loiacono,

Neupert

et al. 2023

Nucleic Acids Research

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“…"RNA thermometers", perhaps aided by KREH2, may regulate editing in response to shifts in temperature and intracellular conditions. Thermometers in trypanosomes, as in other systems, including in plants and chloroplast in green alga (74,75), could influence mRNA and or gRNA secondary structure, or RNA helicase conformation, masking or promoting productive RNA hybrids, cognate or non-cognate. Interestingly, temperature reduction promoted editing efficiency of some cytochrome mRNAs.…”

Section: Rna Conformation In the Nd7 3' Early Checkpoint May Hinder P...mentioning

confidence: 99%

KREH2 helicase represses ND7 mRNA editing in procyclic-stageTrypanosoma bruceiby opposite modulation of canonical and “moonlighting” gRNA utilization creating a proposed mRNA structure

Meehan,

Ivens,

Grote

et al. 2024

Preprint

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Unknown factors regulate mitochondrial U-insertion/deletion (U-indel) RNA editing in procyclic-form (PCF) and bloodstream-form (BSF) trypanosomes. This editing is directed by anti-sense gRNAs, creates canonical protein-encoding mRNAs, and may developmentally control respiration. Canonical editing by housekeeping cognate gRNAs occurs amid massive non-canonical editing of unclear sources and biological significance. We found PCF-specific repression in mRNA ND7 that involves novel modulation of gRNA usage by RNA helicase KREH2. At a major early checkpoint near the mRNA 3' terminus, KREH2 promotes the usage of a non-cognate "terminator" gRNA over a cognate gRNA. At this early checkpoint, terminator-directed editing installs a structural element in 30% of the ND7 transcriptome, which potentially occludes the mRNA 3' terminus and represses further editing. BSF-to-PCF differentiation in vitro recreated this form of negative control. Remarkably, KREH2-RNAi knockdown relieved repression by reverting the native usage of cognate/non-cognate gRNAs at the major early checkpoint. ND7 transcripts that lacked terminator-directed editing at the early checkpoint exhibited similar negative editing control along the mRNA sequence, suggesting that KREH2 modulates guiding fidelity globally. Thus, KREH2 is a key protein in ND7 developmental editing control involving modulation of gRNA selection and RNA structure installed by a regulatory terminator gRNA.

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“…Temperature is one of the most direct physical parameters that influence RNA structure dynamics, and in turn, thermosensitive RNA structures can be used by a cell to perceive and respond to its temperature environment. Indeed, many thermosensitive RNA structures (RNA thermoswitches) with biological function have been identified in bacteria and viruses (Chowdhury et al , 2006; Thomas et al , 2022), suggesting the temperature responsiveness of RNA secondary structures has been harnessed multiple times during evolution. It was shown that temperature sensitivity of RNA structures is exploited by bacteria to fabricate RNA thermosensing systems that allow a rapid adaptive response to temperature change (Mandin & Johansson, 2020).…”

Section: Variation Of Plant Noncoding Genomesmentioning

confidence: 99%

The plant noncoding transcriptome: a versatile environmental sensor

Chorostecki,

Bologna,

Ariel

2023

The EMBO Journal

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Plant noncoding RNA transcripts have gained increasing attention in recent years due to growing evidence that they can regulate developmental plasticity. In this review article, we comprehensively analyze the relationship between noncoding RNA transcripts in plants and their response to environmental cues. We first provide an overview of the various noncoding transcript types, including long and small RNAs, and how the environment modulates their performance. We then highlight the importance of noncoding RNA secondary structure for their molecular and biological functions. Finally, we discuss recent studies that have unveiled the functional significance of specific long noncoding transcripts and their molecular partners within ribonucleoprotein complexes during development and in response to biotic and abiotic stress. Overall, this review sheds light on the fascinating and complex relationship between dynamic noncoding transcription and plant environmental responses, and highlights the need for further research to uncover the underlying molecular mechanisms and exploit the potential of noncoding transcripts for crop resilience in the context of global warming.

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RNA structure mediated thermoregulation: What can we learn from plants?

Cited by 17 publications

References 66 publications

An RNA thermometer in the chloroplast genome of Chlamydomonas facilitates temperature-controlled gene expression

An RNA thermometer in the chloroplast genome of Chlamydomonas facilitates temperature-controlled gene expression

KREH2 helicase represses ND7 mRNA editing in procyclic-stageTrypanosoma bruceiby opposite modulation of canonical and “moonlighting” gRNA utilization creating a proposed mRNA structure

The plant noncoding transcriptome: a versatile environmental sensor

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