Expression and diversification analysis reveals transposable elements play important roles in the origin of Lycopersicon-specific lncRNAs in tomato

Long noncoding RNAs (lncRNAs) regulate gene expression and biological processes. With the development of high-throughput RNA sequencing technology, lncRNAs have been extensively studied in recent years. Nevertheless, the expression and evolution of lncRNAs in plants remain poorly understood. Here, we identified 413 and 709 multi-exon noncoding transcripts from 353 and 595 loci of the cultivar tomato Heinz1706 and its wild relative LA1589, respectively. Systematic comparison of the sequence and expression of lncRNAs showed that they are poorly conserved in Solanaceae, with only <0.4% lncRNAs present in all sequenced genomes of tomato and potato. Sequence analysis of Lycopersicon-specific lncRNA loci in Solanum lycopersicum and S. pennellii showed that the origins of these molecules are associated with transposable elements (TEs). LncRNA-314, a fruit-specific lncRNA expressed in S. lycopersicum and S. pimpinellifolium, but not in S. pennellii, originated through two evolutionary events: speciation of S. pennellii resulted in insertion of a long terminal repeat (LTR) retrotransposon into chromosome 10 and contributed to most of the transcribed region of lncRNA-314; and a large deletion in Lycopersicon generated the promoter region and part of the transcribed region of lncRNA-314. These results provide novel insights into the evolution of lncRNAs in plants.