The trabecular and compact myocardium of adult vertebrate ventricles are transcriptionally similar despite morphological differences

Abstract

A poorly understood, major event in heart evolution is the convergent prioritization in mammals and birds of compact myocardium over trabecular myocardium. Compact myocardium is thought to facilitate the greater cardiac outputs that distinguish endothermic mammals and birds from ectotherms, but the underlying mechanism remains unclear. We used transcriptomics to investigate whether the compact layer myocardium is intrinsically different from that of the trabecular layer. In the embryonic mouse heart, spatial transcriptomics revealed that 3% of detected genes were differentially expressed between trabecular and compact myocardium. In the adult, this analysis yielded only 0.2% differentially expressed genes. Additionally, the transcriptomes of both embryonic trabecular and compact myocardium greatly differed from those of the adult myocardium. Reanalysis of available single-cell transcriptomes showed relationships between human embryonic and adult trabecular and compact myocardium similar to those in mice. Analysis of new and published transcriptomes from adult zebra finch, zebrafish, and tuna revealed few differentially expressed genes (<0.6%) and no conservation between species. We conclude that the transcriptional states of developing trabecular and compact myocardium do not persist into adulthood. In adult hearts, the compact layer myocardium is not intrinsically different from that of the trabecular layer despite the overt morphological differences.