AUXIN-REGULATED PROMOTER LOOP (APOLO) | Thomas Blein

Long non-coding RNAs as regulators of gene expression

Thu, 05 Aug 2021 17:52:41 +0200

Long non-coding RNAs are emerging as versatile regulators of plant gene expression, acting at the interface between chromatin, transcription and RNA processing. We have characterised lncRNAs that control chromatin conformation and gene expression in response to developmental and environmental signals. APOLO recognises distant genomic loci through R-loop formation and decoys LHP1 to modulate chromatin loops during lateral root development; it also interacts with VIM1 and LHP1 to regulate DNA and histone methylation at YUCCA2 during thermomorphogenesis, a function shared with the sequence-unrelated human UPAT lncRNA. MARS controls the marneral biosynthetic gene cluster by titrating LHP1 in an ABA-dependent manner, promoting a chromatin loop between MRN1 and a distal enhancer, while ARES modulates lateral root architecture through its neighbouring genes.

Related publications

— R-Loop Mediated trans Action of the APOLO Long Noncoding RNA
— The Arabidopsis APOLO and human UPAT sequence-unrelated long noncoding RNAs can modulate DNA and histone methylation machineries in plants
— The lncRNA MARS modulates the epigenetic reprogramming of the marneral cluster in response to ABA
— The long intergenic noncoding RNA ARES modulates root architecture in Arabidopsis

A second axis of our work concerns alternative splicing. ASCO interacts with the splicing regulators NSR and with spliceosome components such as PRP8a and SmD1b, thereby modulating the recognition of specific transcripts. More recently, we identified ACHLYS, a Brassicaceae-conserved lncRNA that interacts with NSRa and GRP7 and modulates biomolecular condensates to regulate alternative splicing during lateral root development.

Related publications

— Nuclear Speckle RNA Binding Proteins Remodel Alternative Splicing and the Non-coding Arabidopsis Transcriptome to Regulate a Cross-Talk Between Auxin and Immune Responses
— The Arabidopsis lncRNA ASCO modulates the transcriptome through interaction with splicing factors
— The long non-coding RNA ACHLYS modulates biomolecular condensates to regulate alternative splicing in root development

Beyond these model mechanisms, we investigate how lncRNAs contribute to specific biological processes and how their modes of action can be generalised. We identified lncRNAs associated with anthocyanin pigmentation in carrot roots, reviewed the roles of lncRNAs in root growth and development, and synthesised their contributions to environmental responses and adaptation and to chromatin regulation across plants.

Related publications

— Insights into long non-coding RNA regulation of anthocyanin carrot root pigmentation
— Regulatory long non-coding RNAs in root growth and development
— From environmental responses to adaptation: the roles of plant lncRNAs
— From non-coding to chromatin regulators: VIVIpary and the rise of lncRNAs in plant biology

Conservation and evolution of lncRNAs

Tue, 03 Aug 2021 18:20:46 +0200

Unlike protein-coding genes, lncRNAs show limited sequence conservation, which makes orthology assignment and functional transfer difficult. We investigate alternative levels of conservation—expression, genomic position, secondary structure and function—to understand how lncRNAs evolve and contribute to plant adaptation. Comparing two Arabidopsis accessions under phosphate starvation, we found that lncRNAs are far more variable between accessions than coding genes, even when their DNA sequence is conserved, and identified ecotype-specific lncRNAs linked to root responses. At the genome-wide level, we analysed the evolutionary age, sequence conservation and transcriptional regulation of Arabidopsis lincRNAs, revealing a root-specific transcription-factor network and distinct selective pressures across lincRNA age classes.

Related publications

— Landscape of the Noncoding Transcriptome Response of Two Arabidopsis Ecotypes to Phosphate Starvation
— Transcription factors KANADI 1, MYB DOMAIN PROTEIN 44, and PHYTOCHROME INTERACTING FACTOR 4 regulate long intergenic noncoding RNAs expressed in Arabidopsis roots

Conservation can also be functional rather than sequence-based. APOLO and the human UPAT lncRNA share neither sequence nor structure, yet both are recognised by the conserved VIM1/LHP1 machinery in plants, illustrating how lncRNA function can be preserved through conserved protein interactions. We have synthesised these findings in reviews on lncRNA conservation and on their contribution to environmental adaptation.

Related publications

— The Arabidopsis APOLO and human UPAT sequence-unrelated long noncoding RNAs can modulate DNA and histone methylation machineries in plants
— From environmental responses to adaptation: the roles of plant lncRNAs

More broadly, the same evolutionary question applies to other multigenic and regulatory loci. In apple, we contributed to a haplotype-resolved analysis of the S-locus showing that long-term balancing selection preserves multigenic S-haplotype architectures despite extensive structural divergence and transposable-element accumulation. This broader perspective will help us connect lncRNA evolution to the evolution of plant genomes, regulatory sequences and adaptive traits.

Related publications

— Innovation within stability: balancing selection preserves multigenic S-haplotype architecture in apple

The Arabidopsis APOLO and human UPAT sequence-unrelated long noncoding RNAs can modulate DNA and histone methylation machineries in plants

Mon, 01 Aug 2022 00:00:00 +0000

R-Loop Mediated trans Action of the APOLO Long Noncoding RNA

Sun, 01 Mar 2020 00:00:00 +0000