Development of an inducible DNA barcoding system to understand lineage changes in Arabidopsis regeneration

Plants demonstrate a high degree of developmental plasticity, capable of regenerating entire individuals from detached somatic tissues—a regenerative phenomenon rarely observed in metazoa. Consequently, elucidating the lineage relationship between somatic founder cells and descendant cells in regenerated plant organs has long been a pursuit. In this study, we developed and optimized both DNA barcode- and multi-fluorescence-based cell-lineage tracing toolsets, employing an inducible method to mark individual cells in Arabidopsis donor somatic tissues at the onset of regeneration. Utilizing these complementary methods, we scrutinized cell identities at the single-cell level and presented compelling evidence that all cells in the regenerated Arabidopsis plants, irrespective of their organ types, originated from a single progenitor cell in the donor somatic tissue. Our discovery suggests a single-cell passage directing the transition from multicellular donor tissue to regenerated plants, thereby creating opportunities for cell-cell competition during plant regeneration—a strategy for maximizing survival. [Display omitted] •Generation of cell-lineage tracing toolsets•Lineage tracing reveals the single-cell origin of Arabidopsis regeneration•Lineage tracing reveals the multicellular origin of lateral root development Lu and Zhang et al. investigate the cell-lineage relationship of regenerated Arabidopsis plants. They demonstrate that the regenerated plant originated from a single somatic cell within the donor tissue.