Exploration and dissection of potential actions and effects of long noncoding RNA (lncRNA) in animals remain challenging. Here, using multiple knockout mouse models and single cell RNA sequencing, we demonstrate that the divergent lncRNA / has a key complex modulatory effect on the expression of its neighboring gene and subsequently on heart development and function. Short deletion of the promoter in mouse diminishes transcription to ∼8-32%, but fails to affect 2 expression and yields no discernable heart phenotypes. Interestingly, full-length deletion of in mouse causes moderate yet prevalent upregulation of in hundreds of cardiac cells, leading to profound biological consequences, including dysregulated cardiac gene programs, congenital heart defects and perinatal lethality. We propose that the locus dampens expression to restrain cardiomyocyte proliferation, thereby orchestrating a balanced development of cardiac cell lineages. This study highlights the regulatory complexity of the lncRNA on expression, emphasizing the need for complementary genetic and single cell approaches to delineate the function and primary molecular effects of an lncRNA in animals.
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