Orchestration of Thiamin Biosynthesis and Central Metabolism by Combined Action of the Thiamin Pyrophosphate Riboswitch and the Circadian Clock in <i>Arabidopsis</i>

Bocobza, Samuel; Malitsky, Sergey; Araújo, Wagner L.; Nunes‐Nesi, Adriano; Meir, Sagit; Shapira, Michael Y.; Fernie, Alisdair R.; Aharoni, Asaph

doi:10.1105/tpc.112.106385

Cited by 102 publications

(227 citation statements)

References 73 publications

(101 reference statements)

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“…First, it appears that a single point mutation in the THI4 riboswitch is sufficient to considerably increase B 1 vitamer levels in this alga. This is significant because a recent study in the model plant Arabidopsis showed that the equivalent mutation in the THIC riboswitch affects only the TMP levels, with a threefold change (31). In our study on Chlamydomonas, all three vitamers are increased 5-10-fold (Fig.…”

Section: Discussionsupporting

confidence: 55%

Analysis of Chlamydomonas thiamin metabolism in vivo reveals riboswitch plasticity

Moulin

Nguyen

Scaife

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Thiamin (vitamin B 1 ) is an essential micronutrient needed as a cofactor for many central metabolic enzymes. Animals must have thiamin in their diet, whereas bacteria, fungi, and plants can biosynthesize it de novo from the condensation of a thiazole and a pyrimidine moiety. Although the routes to biosynthesize these two heterocycles are not conserved in different organisms, in all cases exogenous thiamin represses expression of one or more of the biosynthetic pathway genes. One important mechanism for this control is via thiamin-pyrophosphate (TPP) riboswitches, regions of the mRNA to which TPP can bind directly, thus facilitating fine-tuning to maintain homeostasis. However, there is little information on how modulation of riboswitches affects thiamin metabolism in vivo. Here we use the green alga, Chlamydomonas reinhardtii, which regulates both thiazole and pyrimidine biosynthesis with riboswitches in the THI4 (Thiamin 4) and THIC (Thiamin C) genes, respectively, to investigate this question. Our study reveals that regulation of thiamin metabolism is not the simple dogma of negative feedback control. Specifically, balancing the provision of both of the heterocycles of TPP appears to be an important requirement. Furthermore, we show that the Chlamydomonas THIC riboswitch is controlled by hydroxymethylpyrimidine pyrophosphate, as well as TPP, but with an identical alternative splicing mechanism. Similarly, the THI4 gene is responsive to thiazole. The study not only provides insight into the plasticity of the TPP riboswitches but also shows that their maintenance is likely to be a consequence of evolutionary need as a function of the organisms' environment and the particular pathway used.eukaryotic riboswitch | gene expression coordination | metabolic regulation | cross-talk

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Section: Discussionsupporting

confidence: 55%

Analysis of Chlamydomonas thiamin metabolism in vivo reveals riboswitch plasticity

Moulin

Nguyen

Scaife

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Recent studies on thiamine metabolism in photosynthetic organisms have revealed complex regulatory mechanisms involving a riboswitch located on the ThiC pre-mRNA and the presence of regulatory elements located in the 59 upstream sequence of this gene responsible for circadian control of transcription (Bocobza et al, 2013). In addition, a link between stimulation of thiamine biosynthesis under stress and the induction of mRNA for TK and other TPP-requiring enzymes was recently reported (Rapala- Kozik et al, 2012).…”

Section: Resultsmentioning

confidence: 99%

“…This could simply be a consequence of the slow-growth phenotype of these plants. However, starch and chlorotic phenotypes have been observed in plants with altered thiamine metabolism, even in those where growth was not reduced and that possessed an increased capacity for TPP biosynthesis (Bocobza et al, 2013). Plants expressing a ThiC gene with a mutated riboswitch that was insensitive to TPP had starch grains with altered structure, suggesting a change in the process of starch biosynthesis.…”

Section: Tkox Plants Display Compromised Carbon Allocation To the Isomentioning

confidence: 99%

Overexpression of Plastid Transketolase in Tobacco Results in a Thiamine Auxotrophic Phenotype

et al. 2015

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To investigate the effect of increased plastid transketolase on photosynthetic capacity and growth, tobacco (Nicotiana tabacum) plants with increased levels of transketolase protein were produced. This was achieved using a cassette composed of a full-length Arabidopsis thaliana transketolase cDNA under the control of the cauliflower mosaic virus 35S promoter. The results revealed a major and unexpected effect of plastid transketolase overexpression as the transgenic tobacco plants exhibited a slow-growth phenotype and chlorotic phenotype. These phenotypes were complemented by germinating the seeds of transketolase-overexpressing lines in media containing either thiamine pyrophosphate or thiamine. Thiamine levels in the seeds and cotyledons were lower in transketolase-overexpressing lines than in wild-type plants. When transketolaseoverexpressing plants were supplemented with thiamine or thiamine pyrophosphate throughout the life cycle, they grew normally and the seed produced from these plants generated plants that did not have a growth or chlorotic phenotype. Our results reveal the crucial importance of the level of transketolase activity to provide the precursor for synthesis of intermediates and to enable plants to produce thiamine and thiamine pyrophosphate for growth and development. The mechanism determining transketolase protein levels remains to be elucidated, but the data presented provide evidence that this may contribute to the complex regulatory mechanisms maintaining thiamine homeostasis in plants.

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“…This negative feedback regulation of thiamine biosynthesis at the AS level ensures a high level of transcripts under low cellular TPP concentrations. Plants expressing THIC with a disrupted TPP riboswitch in a thic mutant showed growth retardation, chlorosis, and delayed flowering, indicating the physiological significance of riboswitch-mediated regulation of THIC (Bocobza et al, 2013). It is not known to what extent riboswitches regulate AS of other pre-mRNAs in plants.…”

Section: Regulation Of As By Secondary Structuresmentioning

confidence: 99%

Complexity of the Alternative Splicing Landscape in Plants

et al. 2013

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Alternative splicing (AS) of precursor mRNAs (pre-mRNAs) from multiexon genes allows organisms to increase their coding potential and regulate gene expression through multiple mechanisms. Recent transcriptome-wide analysis of AS using RNA sequencing has revealed that AS is highly pervasive in plants. Pre-mRNAs from over 60% of intron-containing genes undergo AS to produce a vast repertoire of mRNA isoforms. The functions of most splice variants are unknown. However, emerging evidence indicates that splice variants increase the functional diversity of proteins. Furthermore, AS is coupled to transcript stability and translation through nonsense-mediated decay and microRNA-mediated gene regulation. Widespread changes in AS in response to developmental cues and stresses suggest a role for regulated splicing in plant development and stress responses. Here, we review recent progress in uncovering the extent and complexity of the AS landscape in plants, its regulation, and the roles of AS in gene regulation. The prevalence of AS in plants has raised many new questions that require additional studies. New tools based on recent technological advances are allowing genome-wide analysis of RNA elements in transcripts and of chromatin modifications that regulate AS. Application of these tools in plants will provide significant new insights into AS regulation and crosstalk between AS and other layers of gene regulation.

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Orchestration of Thiamin Biosynthesis and Central Metabolism by Combined Action of the Thiamin Pyrophosphate Riboswitch and the Circadian Clock in Arabidopsis

Cited by 102 publications

References 73 publications

Analysis of Chlamydomonas thiamin metabolism in vivo reveals riboswitch plasticity

Analysis of Chlamydomonas thiamin metabolism in vivo reveals riboswitch plasticity

Overexpression of Plastid Transketolase in Tobacco Results in a Thiamine Auxotrophic Phenotype

Complexity of the Alternative Splicing Landscape in Plants

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