Long non-coding RNAs underlie multiple domestication traits and leafhopper resistance

The origination and functionality of long non-coding RNAs (lncRNAs) remain poorly understood. Here, we show that multiple quantitative trait loci modulating distinct domestication traits in soybeans are pleiotropic effects of a locus composed of two tandem lncRNA genes. These lncRNA genes, each containing two inverted repeats (IRs) originated from coding sequences of MYB genes, function by generating clusters of small RNAs in wild soybeans to inhibit the expression of their MYB gene relatives through posttranscriptional regulation. In contrast, the expression of the lncRNA genes in cultivated soybeans is severely repressed, and consequently, the corresponding MYB genes are highly expressed, shaping multiple distinct domestication traits as well as leafhopper resistance. The IRs were formed before the divergence of the Glycine genus from the Phaseolus/Vigna lineage and exhibit strong structure-function constraints. This study exemplifies a new type of targets for selection during plant domestication and uncovers mechanisms of lncRNA formation and action.