An Intracellular Transcriptomic Atlas of the Giant Coenocyte Caulerpa taxifolia

Convergent morphologies have arisen in plants multiple times. In non-vascular and vascular land plants, convergent morphology in the form of roots, stems, and leaves arose. The morphology of some green algae includes an anchoring holdfast, stipe, and leaf-like fronds. Such morphology occurs in the absence of multicellularity in the siphonous algae, which are single cells. Morphogenesis is separate from cellular division in the land plants, which although are multicellular, have been argued to exhibit properties similar to single celled organisms. Within the single, macroscopic cell of a siphonous alga, how are transcripts partitioned, and what can this tell us about the development of similar convergent structures in land plants? Here, we present a de novo assembled, intracellular transcriptomic atlas for the giant coenocyte Caulerpa taxifolia. Transcripts show a global, basal-apical pattern of distribution from the holdfast to the frond apex in which transcript identities roughly follow the flow of genetic information in the cell, transcription-to-translation. The analysis of the intersection of transcriptomic atlases of a land plant and Caulerpa suggests the recurrent recruitment of transcript accumulation patterns to organs over large evolutionary distances. Our results not only provide an intracellular atlas of transcript localization, but also demonstrate the contribution of transcript partitioning to morphology, independent from multicellularity, in plants.Author Summary: Plants include both the green algae and land plants. Multiple times, root, stem, and leaf-like structures arose independently in plant lineages. In some instances, such as the siphonous algae, these structures arose in the absence of multicellularity. It has been argued by some that the morphology of multicellular land plant organs similarly arises independently of cell division patterns. Here, we explore the partitioning of gene transcripts within what is debatably the largest single-celled organism in the world, the siphonous alga Caulerpa taxifolia. We find that within this giant cell specific transcripts localize within pseudo-organs (morphological structures that are not comprised of cells or tissue). The overall pattern of transcript accumulation follows an apical-basal pattern within the cell. Moreover, transcripts related to different cellular processes, such as transcription and translation, localize to specific regions. Analyzing the signatures of transcript accumulation in land plant organs and the pseudo-organs of Caulerpa, we find that groups of transcripts accumulate together in morphological structures across evolution at rates higher than expected by chance. Together, our results demonstrate a relationship between transcript partitioning and organism morphology, independent from multicellularity, throughout diverse plant lineages.