To gain their unique biological function, plant cells regulate protein biosynthesis through gene activation and repression along with multiple mRNA mechanisms. The subcellular localization of mRNAs has been reported as a complementary regulatory mechanism of the biology of fungi, yeast, and animal cells. However, studies comprehensively reporting the impact of mRNA localization in plant cells are lacking.

Here, we set to mathematically model the spatial distribution of sub-cellular cytosolic transcripts across multiple cell types and developmental stages. Through the use of high-resolution spatial transcriptomic technology, we first report the comprehensive and differential mapping of millions of plant transcripts between the nuclear and cytoplasmic compartments of various soybean nodule cell types. We then characterize key mathematical features of these transcriptomic spatial distributions using Topological Data Analysis (TDA). TDA offers a comprehensive pattern-quantifying framework that is robust to variations in cell shape, size, and orientation. TDA thus provides us with a common ground to mathematically compare and contrast intrinsic differences in sub-cellular transcript distributions and patterns across cell types and expressed genes.

Our analyses reveal distinct patterns and spatial distributions of plant transcripts between the nucleus and cytoplasm, varying both between and within genes, as well as across different cell types. We believe this differential distribution is an additional, less understood, regulatory mechanism controlling protein translation and localization, cell identity, and cell state and reveals the influence of the sub-compartmentalization of transcripts as another post-transcriptional regulatory mechanism.