Long non-coding RNAs (lncRNAs) have emerged as crucial modifiers of eukaryotic transcriptomes. In plant systems, lncRNAs have been demonstrated to act as transcriptional integrators and regulators of development and stress responses. However, investigation of their conservation within and across plant lineages has been limited by their lack of apparent sequence conservation, a heuristic that is heavily utilized for the exploration of protein-coding genes. To circumvent this complication, we suggest a more informed and nuanced interpretation of conservation can and should be used to elucidate the extent of lncRNA conservation and function in plant systems. Working within Brassicaceae, we use a model plant molecular system Arabidopsis thaliana, as a point of reference and Brassica rapa (R-o-18), a model crop species and close relative of Arabidopsis thaliana to define a comparative transcriptomic framework for exploring the similarity and variability in the transcriptional networks that govern plant development in these two species. Specifically, we present a comprehensive tissue atlas for Brassica rapa (R-o-18), a mesopolyploid model for polyploid studies, an agronomically significant oilseed crop, and close relative of Arabidopsis thaliana. Utilizing integrated Illumina and Nanopore direct RNA-sequencing across 22 tissues and developmental stages, we significantly improved the R-o-18 annotation, identifying over 3,500 putative novel protein coding genes (PCGs) and over 8,100 long non-coding RNAs (lncRNAs). Demonstrating the utility of this resource we define and characterize the extent of divergence of regulatory programs in Arabidopsis and Brassica, specifically in the transcriptional networks that govern germinating seed. Finally, we define and characterize “transcriptionally analogous lncRNAs”, transcripts that lack sequence homology yet occupy conserved network nodes, exhibit similar expression profiles across species, and contain similar enriched k-mer motifs. This work provides an expanded genomic resource for the Brassica community, a comparative transcriptomic resource for Arabidopsis researchers, and establishes a functional framework for identifying analogous non-coding RNA regulators across divergent plant lineage.