Gibberellins promote polar auxin transport to regulate stem cell fate decisions in cambium

Abstract

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.

Gibberellin promotes cambium reestablishment during secondary vascular tissue regeneration after girdling in an auxin‐dependent manner in Populus

“…Moreover, the 35S:PtoGAI plants showed inhibited proliferation and differentiation of the vascular cambium, as well as inhibition of the transition from primary vascular tissue to SVT (Figure 4E, F). Previous studies also found that cambium-specific promoter-driven degradationresistant versions of RGL1 (pWOX4a:ΔRGL1) or RGA (pANT: ΔRGA17) inhibited cambium division and xylem differentiation (Hu et al, 2022;Mäkilä et al, 2023). Therefore, overexpression of DELLAs or inhibition of DELLA degradation suppresses the proliferation of cambium and differentiation into xylem.…”

“…The PIN auxin efflux carriers act primarily in controlling how auxin accumulates in various tissues during plant development (Adamowski and Friml, 2015). It has been reported that GA regulates PIN transcription in the root apical meristem and vascular cambium (Björklund et al, 2007; Willige et al, 2011; Löfke et al, 2013; Mäkilä et al, 2023). In the vascular tissues of unpeeled Populus , PIN1 is predominantly localized in the cambial regions (Figure S8), which is consistent with the results observed in Arabidopsis (Gälweiler et al, 1998).…”

“…Our results show that GA is involved in the feed‐forward loop of auxin signaling during SVT regeneration, by promoting the ARF‐mediated auxin response and enhancing the expression pattern of PIN1 (Figures 5, 6). During SVT development, GA can promote the expression of auxin‐responsive genes and PIN1‐regulated polar auxin transport in the absence of exogenous hormone application (Hu et al, 2022; Mäkilä et al, 2023). However, GA alone cannot activate the expression of auxin transport and response genes, so it cannot induce SVT regeneration in the in vitro system.…”

“…Auxin response factors and auxin efflux carrier PIN1 form a feed-forward loop to regulate the development of vascular tissues. PIN1 promotes the accumulation of auxin in vascular stem cells in roots, thereby upregulating ARF-mediated auxin signaling (Mäkilä et al, 2023). During poplar SVT development, auxin-induced ARF7 can directly bind to the promoter of PIN1 to activate its expression and amplify auxin signaling (Hu et al, 2022).…”

“…Auxin degrades AUX/IAA proteins and GA destabilizes DELLA proteins, which removes their inhibitory effect on ARF7 and promotes the ability of cambium to proliferate and differentiate (Hu et al, 2022). In addition, GA alters the direction of stem cell differentiation toward the xylem and phloem in vascular tissue; it increases the maximum auxin concentration of the xylem side by promoting PIN1‐dependent polar auxin transport, resulting in preferential differentiation of stem cells into the xylem (Mäkilä et al, 2023). Moreover, GA represses phloem proliferation by reducing the inhibitory effect of DELLA proteins on ARF6 and ARF8 (Ben‐Targem et al, 2021).…”