LncRNA FLAIL Affects Alternative Splicing and Represses Flowering in Arabidopsis

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2023 Apr 13

PMID 37051749

Authors

Yu Jin

Maxim Ivanov

Anna Nelson Dittrich

Andrew Dl Nelson

Sebastian Marquardt

Affiliations

Soon will be listed here.

Abstract

How the noncoding genome affects cellular functions is a key biological question. A particular challenge is to distinguish the effects of noncoding DNA elements from long noncoding RNAs (lncRNAs) that coincide at the same loci. Here, we identified the flowering-associated intergenic lncRNA (FLAIL) in Arabidopsis through early flowering flail mutants. Expression of FLAIL RNA from a different chromosomal location in combination with strand-specific RNA knockdown characterized FLAIL as a trans-acting RNA molecule. FLAIL directly binds to differentially expressed target genes that control flowering via RNA-DNA interactions through conserved sequence motifs. FLAIL interacts with protein and RNA components of the spliceosome to affect target mRNA expression through co-transcriptional alternative splicing (AS) and linked chromatin regulation. In the absence of FLAIL, splicing defects at the direct FLAIL target flowering gene LACCASE 8 (LAC8) correlated with reduced mRNA expression. Double mutant analyses support a model where FLAIL-mediated splicing of LAC8 promotes its mRNA expression and represses flowering. Our study suggests lncRNAs as accessory components of the spliceosome that regulate AS and gene expression to impact organismal development.

Citing Articles

Nanopore direct RNA sequencing reveals N-methyladenosine and polyadenylation landscapes on long non-coding RNAs in Arabidopsis thaliana.

Liang Q, Zhang J, Lam H, Chan T BMC Plant Biol. 2024; 24(1):1126.

PMID: 39592939 PMC: 11590578. DOI: 10.1186/s12870-024-05845-4.

CANTATAdb 3.0: An Updated Repository of Plant Long Non-Coding RNAs.

Szczesniak M, Wanowska E Plant Cell Physiol. 2024; 65(9):1486-1493.

PMID: 39018027 PMC: 11447640. DOI: 10.1093/pcp/pcae081.

Update on functional analysis of long non-coding RNAs in common crops.

Zhang A, Pi W, Wang Y, Li Y, Wang J, Liu S Front Plant Sci. 2024; 15:1389154.

PMID: 38872885 PMC: 11169716. DOI: 10.3389/fpls.2024.1389154.

Predicted roles of long non-coding RNAs in abiotic stress tolerance responses of plants.

Imaduwage I, Hewadikaram M Mol Hortic. 2024; 4(1):20.

PMID: 38745264 PMC: 11094901. DOI: 10.1186/s43897-024-00094-3.

Exploring the Regulatory Dynamics of -Associated lncRNA in Modulating the Flowering Response of Chinese Cabbage.

Dai Y, Gao X, Zhang S, Li F, Zhang H, Li G Int J Mol Sci. 2024; 25(3).

PMID: 38339202 PMC: 10856242. DOI: 10.3390/ijms25031924.

References

Severing E, Faino L, Jamge S, Busscher M, Kuijer-Zhang Y, Bellinazzo F . Arabidopsis thaliana ambient temperature responsive lncRNAs. BMC Plant Biol. 2018; 18(1):145. PMC: 6045843. DOI: 10.1186/s12870-018-1362-x. View

Thomas Q, Ard R, Liu J, Li B, Wang J, Pelechano V . Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis. Nat Commun. 2020; 11(1):2589. PMC: 7244574. DOI: 10.1038/s41467-020-16390-7. View

Fang J, Zhang F, Wang H, Wang W, Zhao F, Li Z . locus shortens rice maturity duration without yield penalty. Proc Natl Acad Sci U S A. 2019; 116(37):18717-18722. PMC: 6744900. DOI: 10.1073/pnas.1815030116. View

Kindgren P, Ard R, Ivanov M, Marquardt S . Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nat Commun. 2018; 9(1):4561. PMC: 6212407. DOI: 10.1038/s41467-018-07010-6. View

Xiao J, Li C, Xu S, Xing L, Xu Y, Chong K . JACALIN-LECTIN LIKE1 Regulates the Nuclear Accumulation of GLYCINE-RICH RNA-BINDING PROTEIN7, Influencing the RNA Processing of FLOWERING LOCUS C Antisense Transcripts and Flowering Time in Arabidopsis. Plant Physiol. 2015; 169(3):2102-17. PMC: 4634062. DOI: 10.1104/pp.15.00801. View

Yap K, Mukhina S, Zhang G, Tan J, Ong H, Makeyev E . A Short Tandem Repeat-Enriched RNA Assembles a Nuclear Compartment to Control Alternative Splicing and Promote Cell Survival. Mol Cell. 2018; 72(3):525-540.e13. PMC: 6224606. DOI: 10.1016/j.molcel.2018.08.041. View

Tellier M, Maudlin I, Murphy S . Transcription and splicing: A two-way street. Wiley Interdiscip Rev RNA. 2020; 11(5):e1593. DOI: 10.1002/wrna.1593. View

Cai X, Davis E, Ballif J, Liang M, Bushman E, Haroldsen V . Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot. 2006; 57(11):2563-9. DOI: 10.1093/jxb/erl022. View

Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D . Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell. 2006; 18(5):1121-33. PMC: 1456875. DOI: 10.1105/tpc.105.039834. View

10.

Wu M, Yang L, Chen L . Long noncoding RNA and protein abundance in lncRNPs. RNA. 2021; 27(12):1427-1440. PMC: 8594465. DOI: 10.1261/rna.078971.121. View

11.

Seo J, Sun H, Park B, Huang C, Yeh S, Jung C . ELF18-INDUCED LONG-NONCODING RNA Associates with Mediator to Enhance Expression of Innate Immune Response Genes in Arabidopsis. Plant Cell. 2017; 29(5):1024-1038. PMC: 5466027. DOI: 10.1105/tpc.16.00886. View

12.

Shi Y, Zhang X, Xu Z, Li L, Zhang C, Schlappi M . Influence of EARLI1-like genes on flowering time and lignin synthesis of Arabidopsis thaliana. Plant Biol (Stuttg). 2011; 13(5):731-9. DOI: 10.1111/j.1438-8677.2010.00428.x. View

13.

Beilstein M, Nagalingum N, Clements M, Manchester S, Mathews S . Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2010; 107(43):18724-8. PMC: 2973009. DOI: 10.1073/pnas.0909766107. View

14.

Sun L, van Nocker S . Analysis of promoter activity of members of the PECTATE LYASE-LIKE (PLL) gene family in cell separation in Arabidopsis. BMC Plant Biol. 2010; 10:152. PMC: 3017822. DOI: 10.1186/1471-2229-10-152. View

15.

Heo J, Sung S . Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science. 2010; 331(6013):76-9. DOI: 10.1126/science.1197349. View

16.

Engreitz J, Sirokman K, McDonel P, Shishkin A, Surka C, Russell P . RNA-RNA interactions enable specific targeting of noncoding RNAs to nascent Pre-mRNAs and chromatin sites. Cell. 2014; 159(1):188-199. PMC: 4177037. DOI: 10.1016/j.cell.2014.08.018. View

17.

Bernard D, Prasanth K, Tripathi V, Colasse S, Nakamura T, Xuan Z . A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 2010; 29(18):3082-93. PMC: 2944070. DOI: 10.1038/emboj.2010.199. View

18.

Guo J, Fang S, Wu Y, Zhang J, Chen Y, Liu J . CNIT: a fast and accurate web tool for identifying protein-coding and long non-coding transcripts based on intrinsic sequence composition. Nucleic Acids Res. 2019; 47(W1):W516-W522. PMC: 6602462. DOI: 10.1093/nar/gkz400. View

19.

Aslanzadeh V, Huang Y, Sanguinetti G, Beggs J . Transcription rate strongly affects splicing fidelity and cotranscriptionality in budding yeast. Genome Res. 2017; 28(2):203-213. PMC: 5793784. DOI: 10.1101/gr.225615.117. View

20.

Morlando M, Ballarino M, Gromak N, Pagano F, Bozzoni I, Proudfoot N . Primary microRNA transcripts are processed co-transcriptionally. Nat Struct Mol Biol. 2009; 15(9):902-9. PMC: 6952270. DOI: 10.1038/nsmb.1475. View