The functional balance between the <i>WUSCHEL-RELATED HOMEOBOX1</i> gene and the phytohormone auxin is a key factor for cell proliferation in Arabidopsis seedlings

Abstract

The WUSCHEL-RELATED HOMEOBOX1 (WOX1) transcription factor and its homolog PRESSED FLOWER (PRS) are multifunctional regulators of leaf development that act as transcriptional repressors. These genes promote cell proliferation under certain conditions, but the related molecular mechanisms are not well understood. Here, we present a new function for WOX1 in cell proliferation. To identify the WOX1 downstream genes, we performed a microarray analysis of shoot apices of transgenic Arabidopsis thaliana lines harboring [35Sp::WOX1-glucocorticoid receptor (GR)] in which the WOX1 function was temporarily enhanced by dexamethasone. The downregulated genes were significantly enriched for the Gene Ontology term "response to auxin stimulus", whereas the significantly upregulated genes contained auxin transport-associated PIN1 and AUX1 and the auxin response factor MP, which are involved in formation of auxin response maxima. Simultaneous treatments of synthetic auxin and dexamethasone induced the formation of green compact calli and the unorganized proliferation of cells in the hypocotyl. A microarray analysis of 35Sp::WOX1-GR plants treated with indole-3-acetic acid and dexamethasone revealed that WOX1 and auxin additively influenced their common downstream genes. Furthermore, in the presence of an auxin-transport inhibitor, cell proliferation during leaf initiation was suppressed in the prs mutant but induced in a broad region of the peripheral zone of the shoot apical meristem in the ectopic WOX1expressing line FILp::WOX1. Thus, our results clarify the additive effect of WOX1/PRS and auxin on their common downstream genes and highlight the importance of the balance between their functions in controlling cell proliferation.

GAL4/GFP enhancer‐trap lines for identification and manipulation of cells and tissues in developing Arabidopsis leaves

“…These observations suggest that, at least in part, it is the increased auxin signaling in the cells that normally differentiate into vein elements that leads the flanking cells, which normally would not differentiate into such elements, to do in fact so. Our conclusion is consistent with interpretations of similar findings in other plant organs (eg, References 70‐74) and, more in general, with organ‐specific interpretations of genetic mosaics that span multiple organs in other organisms (eg, References 75‐77). Nevertheless, we cannot rule out an effect on leaf vein patterning of increased auxin signaling in the vascular tissue of nonleaf organs, where E2331>>erGFP is also expressed (Figure 5H,Q,Z); in the future, that possibility will have to be addressed by complementary approaches such as clonal analysis (eg, References 78, 79).…”

Auxin and Flower Development: A Blossoming Field

“…In leaf primordia, auxin up-regulates PRS and its paralogue WOX1 (Caggiano et al 2017) via MP (Guan et al 2017). Increased expression of DR5::GFP in the leaf base of prs wox1 and the increased sensitivity of prs leaves to auxin transport inhibitors implies a role for PRS in auxin transport (Nakata et al 2018). By analogy, positive feedback between auxin and PRS might exist during sepal initiation.…”

The Diverse Roles of Auxin in Regulating Leaf Development

“…On the other hand, WOX1 and PRS (and orthologs in other species) regulate auxin levels and auxin response to promote leaf development [53]. A genome-wide analysis found that both upregulated and downregulated genes by WOX1 were enriched with auxin responsive genes [68].…”