LncRNA FLAIL affects alternative splicing and represses flowering in Arabidopsis

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. Synopsis An early flowering mutant screen was used to identify flail , a mutant mapping to a non‐coding region of the genome. This study shows that the locus encodes for the long noncoding RNA FLAIL , which serves as an accessory component of the spliceosome that regulates alternative splicing and gene expression to repress flowering. FLAIL is a trans‐ acting RNA molecule that represses flowering. FLAIL binds to chromatin regions of target genes through conserved sequence motifs. FLAIL interacts with the spliceosome complex to affect target mRNA expression by co‐transcriptional alternative splicing process and regulation of chromatin modifications. FLAIL represses flowering by regulating alternative splicing and inducing mRNA expression of its direct flowering target LAC8 . Graphical Abstract FLAIL is a trans‐ acting lncRNA that targets the spliceosome and regulates plant flowering by promoting expression of the laccase LAC8 .