Light regulates alternative splicing outcomes via the TOR kinase pathway

Riegler, Stefan; Servi, Lucas; Scarpin, M Regina; Herz, Micaela Amalia Godoy; Kubaczka, M. Guillermina; Venhuizen, Peter; Meyer, Christian; Brunkard, Jacob O.; Kalyna, Maria; Barta, Andrea; Petrillo, Ezequiel

doi:10.1016/j.celrep.2021.109676

Cited by 42 publications

(47 citation statements)

References 48 publications

(86 reference statements)

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“…This glycolysis-dependent promotion of TOR activity could be a specificity of heterotrophic tissues that allows a systemic integration of developmental progression with shoot photosynthetic capacity. Such coupling has been reported for the light-dependent regulation of alternative splicing in roots which is triggered by shoot-photosynthesized sugars and compromised when TOR levels are reduced or its activity reduced (Riegler et al , 2021).…”

Section: Resultsmentioning

confidence: 65%

TOR acts as metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana

Stitz

Kuster

Reinert

et al. 2022

Preprint

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Plants post-embryonic organogenesis requires matching the available metabolic resources to the developmental programs. The root system is determined by the formation of lateral roots (LR), which in Arabidopsis thaliana entails the auxin-induced activation of founder cells located in the pericycle. While the allocation of sugars to roots influences root branching, how sugar availability is sensed for auxin-triggered formation of LRs remains unknown. Here, we combine metabolic profiling with cell-specific genetic interference to show that LR formation is an important sink for carbohydrate accompanied by a switch to glycolysis. We show that the target-of-rapamycin (TOR) kinase is locally activated in the pericycle and the founder cells and that both chemical and genetic inhibition of TOR kinase lead to a block of LR initiation. TOR marginally affects the auxin-induced transcriptional response of the pericycle but modulates the translation of ARF19, ARF7 and LBD16, three key targets of auxin signalling. These data place TOR as a gatekeeper for post-embryonic LR formation that integrates local auxin-dependent pathways with systemic metabolic signals, modulating the translation of auxin induced gene expression.

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Section: Resultsmentioning

confidence: 65%

TOR acts as metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana

Stitz

Kuster

Reinert

et al. 2022

Preprint

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“…Thus, effective retrograde communication and its linkages with RNA metabolism have been extensively studied [ 76 ]. For example, it was demonstrated that changes in the PQ redox pool may regulate the alternative splicing process [ 38 , 77 , 78 ]. Recently, the basis of these mechanisms was revealed, showing that light increases the PolII elongation rate, while in darkness, elongation is reduced, which is consistent with the kinetic coupling model also found in mammalian cells [ 79 , 80 ].…”

Section: Discussionmentioning

confidence: 99%

Plastid retrograde regulation of miRNA expression in response to light stress

et al. 2022

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Background MicroRNAs (miRNAs) are a class of endogenous noncoding RNAs that play a pivotal role in the regulation of plant development and responses to the surrounding environment. Despite the efforts made to elucidate their function in the adaptation of plants to many abiotic and biotic stresses, their role in high light (HL) stress is still vague. HL stress often arises upon plant exposure to full sunlight. Subsequent changes in nuclear gene expression are triggered by chloroplast-derived retrograde signals. Results In this study, we show that HL is involved in miRNA-dependent regulation in Arabidopsis thaliana rosettes. Microtranscriptomic screening revealed a limited number of miRNAs reacting to HL. To explain the miRNA regulation mechanisms at the different biogenesis stages, chemical and genetic approaches were applied. First, we tested the possible role of plastoquinone (PQ) redox changes using photosynthetic electron transport chain inhibitors. The results suggest that increased primary transcript abundance (pri-miRNAs) of HL-regulated miRNAs is dependent on signals upstream of PQ. This indicates that such signals may originate from photosystem II, which is the main singlet oxygen (1O2) source. Nevertheless, no changes in pri-miRNA expression upon a dark–light shift in the conditional fluorescent (flu) mutant producing 1O2 were observed when compared to wild-type plants. Thus, we explored the 1O2 signaling pathway, which is initiated independently in HL and is related to β-carotene oxidation and production of volatile derivatives, such as β-cyclocitral (β-CC). Pri-miRNA induction by β-CC, which is a component of this 1O2 pathway, as well as an altered response in the methylene blue sensitivity 1 (mbs1) mutant support the role of 1O2 signaling in miRNA regulation. Conclusions We show that light stress triggers changes in miRNA expression. This stress response may be regulated by reactive oxygen species (ROS)-related signaling. In conclusion, our results link ROS action to miRNA biogenesis, suggesting its contribution to inconsistent pri- and mature miRNA dynamics.

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“…These studies uncovered extensive light-sensitive AS and APA programs in this plant. Of note, such rhythmic patterns were correlated with gene-level oscillations of factors involved in AS and APA [223,224]. More recently, it was shown that the TOR kinase, homolog of mammalian mTOR, modulates a specific splicing program in response to light.…”

Section: The Circadian Clock Pathway and Rna Processing Regulationmentioning

confidence: 95%

Coordination of RNA Processing Regulation by Signal Transduction Pathways

2021

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Signal transduction pathways transmit the information received from external and internal cues and generate a response that allows the cell to adapt to changes in the surrounding environment. Signaling pathways trigger rapid responses by changing the activity or localization of existing molecules, as well as long-term responses that require the activation of gene expression programs. All steps involved in the regulation of gene expression, from transcription to processing and utilization of new transcripts, are modulated by multiple signal transduction pathways. This review provides a broad overview of the post-translational regulation of factors involved in RNA processing events by signal transduction pathways, with particular focus on the regulation of pre-mRNA splicing, cleavage and polyadenylation. The effects of several post-translational modifications (i.e., sumoylation, ubiquitination, methylation, acetylation and phosphorylation) on the expression, subcellular localization, stability and affinity for RNA and protein partners of many RNA-binding proteins are highlighted. Moreover, examples of how some of the most common signal transduction pathways can modulate biological processes through changes in RNA processing regulation are illustrated. Lastly, we discuss challenges and opportunities of therapeutic approaches that correct RNA processing defects and target signaling molecules.

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Light regulates alternative splicing outcomes via the TOR kinase pathway

Abstract: Highlights d Chloroplast retrograde signals control alternative splicing in Arabidopsis thaliana d TOR kinase has a central role in alternative splicing control in roots d Mitochondria mediate light/sucrose effects on alternative splicing in roots

Cited by 42 publications

References 48 publications

TOR acts as metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana

TOR acts as metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana

Plastid retrograde regulation of miRNA expression in response to light stress

Coordination of RNA Processing Regulation by Signal Transduction Pathways

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