Wood originates from cell proliferation of the vascular cambium. Xylem (i.e. wood) is produced inside and phloem outside of the cambium 1. Morphogenesis in plants is typically coordinated by organiser cells which direct the adjacent stem cells to undergo programmed cell division and differentiation. It is unknown where the vascular cambium stem cells are located and whether the organiser concept applies to the cambium 2. Here, we combine lineage tracing and molecular genetic studies in Arabidopsis thaliana roots to show that cells with xylem identity direct adjacent vascular cambial cells to divide and function as stem cells. Thus, these xylem identity cells constitute an organiser. A local maximum of the phytohormone auxin and consequent expression of class III homeodomain-leucine zipper (HD-ZIP III) transcription factors promote xylem identity and cellular quiescence of the organiser cells. Additionally, the organiser maintains phloem identity cell nonautonomously. Consistent with this dual function of the organiser cells, xylem and phloem originate from a single, bifacial stem cell in each radial cell file, thus confirming the classical theory of a uniseriate vascular cambium 3. Ectopically activated high auxin signalling clones differentiate as xylem vessels, and induce cell divisions and expression of cambial and phloem markers in the adjacent cells, suggesting that local auxin signalling maximum is sufficient to specify a stem cell organiser. Although vascular cambium has a unique function among plant meristems, its stem cell organiser shares features with the root and shoot meristem organisers.

In plants, the only confirmed function for thermospermine is regulating xylem cells maturation. However, genes putatively encoding thermospermine synthases have been identified in the genomes of both vascular and non-vascular plants. Here, we verify the activity of the thermospermine synthase genes and the presence of thermospermine in vascular and non-vascular land plants as well as in the aquatic plant Chlamydomonas reinhardtii . In addition, we provide information about differential content of thermospermine in diverse organs at different developmental stages in some vascular species that suggest that, although the major role of thermospermine in vascular plants is likely to be xylem development, other potential roles in development and/or responses to stress conditions could be associated to such polyamine. In summary, our results in vascular and non-vascular species indicate that the capacity to synthesize thermospermine is conserved throughout the entire plant kingdom.

Vascular cambium contains bifacial stem cells, which produce secondary xylem to one side and secondary phloem to the other. However, how these fate decisions are regulated is unknown. Here, we show that the positioning of an auxin signalling maximum within the cambium determines the fate of stem cell daughters. The position is modulated by gibberellin-regulated, PIN1-dependent polar auxin transport. Gibberellin treatment broadens auxin maximum from the xylem side of the cambium towards the phloem. As a result, xylem-side stem cell daughter preferentially differentiates into xylem, while phloem-side daughter retains stem cell identity. Occasionally, this broadening leads to direct specification of both daughters as xylem, and consequently, adjacent phloem-identity cell reverts to being stem cell. Conversely, reduced gibberellin levels favour specification of phloem-side stem cell daughter as phloem. Together, our data provide a mechanism by which gibberellin regulates the ratio of xylem and phloem production.