Bifacial cambium stem cells generate xylem and phloem during radial plant growth

Abstract

A reduced rate of stem cell division is considered a widespread feature which ensures the integrity of genetic information during somatic development of plants and animals. Radial growth of plant shoots and roots is a stem cell-driven process that is fundamental for the mechanical and physiological support of enlarging plant bodies. In most dicotyledonous species, the underlying stem cell niche, the cambium, generates xylem inwards and phloem outwards. Despite the importance and intriguing dynamics of the cambium, the functional characterization of its stem cells is hampered by the lack of experimental tools for accessing distinct cambium sub-domains. Here, we use the hypocotyl of Arabidopsis thaliana to map stem cell activity in the proliferating cambium. Through pulse labeling and genetically encoded lineage tracing, we find that a single bifacial stem cell generates both xylem and phloem cell lineages. This cell is characterized by a specific combination of PXY (TDR), SMXL5 and WOX4 gene activity and a high division rate in comparison with tissue-specific progenitors. Our analysis provides a cellular fate map of radial plant growth, and suggests that stem cell quiescence is not a general prerequisite for life-long tissue production.This article has an associated ‘’ interview.

Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth

“…Together, this setup was able to maintain stable radial tissue organization during radial growth and established a maximum of cell division rates in the cambium center as observed by experimental means [12]. Thus, we conclude that cambium organization and radial patterning of plant growth axes can be maintained by a distinct pattern of radially acting morphogens.…”

“…1B, E, F). This pattern was reminiscent of the exclusive activity of the PXY promoter in the proximal cambium area observed previously[12,27]. Thus, although phloem was not produced, with maintaining a circular domain of cambium cells* and cell* proliferation and with promoting xylem* production, Model 1 was able to recapitulate several central features of the active cambium.The combination of PXY and SMXL5 promoter reporters visualizes cambium anatomyTo identify rules for phloem formation, we took advantage of findings obtained using the PXYpro:CYAN FLUORESCENT PROTEIN (PXYpro:CFP) and SUPPRESSOR OF MAX2-LIKE 5pro:YELLOW FLUORESCENT PROTEIN (SMLX5pro:YFP) markers,…”

“…Growth and development of multicellular organisms are complex non-linear processes whose dynamics and network properties are not possible to predict only based on information on their individual building blocks and their one-to-one interactions. The rather simple cellular outline along the radial axes of organs, growth in only two dimensions, and the recent identification of central functional properties [10][11][12], make radial plant growth an attractive target for a systematic approach to reveal its intriguing dynamics. Here, we developed a computational representation of radial plant growth using the VirtualLeaf framework [30] which can recapitulate fundamental features of this process and integrates the PXY/CLE41 module as one central element for cambium patterning and maintenance of tissue domains.…”

“…In the resulting Model 1, the growing structure maintained a circular pool of dividing cambium cells* with a high concentration of PXY-active* while producing xylem cells* toward the center of the organ ( recently established read-outs for cambium anatomy [12]. PXYpro:CFP and SMXL5pro:YFP markers label the proximal and distal cambium domain, respectively, and are therefore indicative of the bipartite cambium organization [12].…”

“…In the resulting Model 1, the growing structure maintained a circular pool of dividing cambium cells* with a high concentration of PXY-active* while producing xylem cells* toward the center of the organ ( recently established read-outs for cambium anatomy [12]. PXYpro:CFP and SMXL5pro:YFP markers label the proximal and distal cambium domain, respectively, and are therefore indicative of the bipartite cambium organization [12]. A transgene expressing the fluorescent mCherry protein under the control of the Histone 4 promoter (H4pro:mCherry) as an approximate marker for cell divisions [31,32], confirmed similar rates of cell proliferation along both domains [12] and revealed that H4pro:mCherry positive cells are present equally in PXYpro:CFP and SMXL5pro:YFP positive regions with the center of activity at the interface of both domains ( Fig.…”