Local auxin biosynthesis promotes shoot patterning and stem cell differentiation in Arabidopsis shoot apex

Abstract

One of the striking aspects of stem cells is their ability to self-renew to maintain the adequate pool over extended periods and differentiate into distinct cell types on demand to sustain the tissue growth and repair by supplying new cells. Arabidopsis plant harbors pluripotent stem cells in the central zone (CZ) of the shoot apex. The daughters of these cells upon cell division move towards the peripheral zone (PZ). At the flanks of the meristem, they form lateral organs. Cells that get displaced underneath CZ become part of the rib-meristem (RM).RM gives rise to stem tissue and vascular cell types in higher plants. Despite the three decades of genetic research work, our understanding of how stem cells differentiate into PZ and RM cell types is inadequate. Here, we show that locally produced auxin in combination with transportis essential for stem cell differentiation and organogenesis in the shoot apex.WUSCHEL, a homeodomain transcription factor, negatively regulates auxin biosynthesis in the stem cell niche to maintain the long-term pluripotency of shoot stem cells. Our findings reveal the role of local auxin biosynthesis in stem cell differentiation and how WUSCHEL regulates auxin signaling to promote stem cell fate in the shoot apex. Main textIn shoot apical meristem (SAM), stem cell proliferation and exit are strictly controlled by cell-cell signaling network controlled by receptor like kinase CLAVATA1 (CLV1) and its ligand CLAVATA3 (CLV3) 1,2 . CLV3 binds to CLV1 and initiates the signaling cascade, which restricts the expression of WUSCHEL (WUS) in the organizing center 3-6 .WUS protein moves from its site of synthesis through plasmodesmata and directly activates CLV3 in CZ and also represses genes involved in differentiation 7-9 .Thus, WUS not only specifies stem cells in apical meristem but also serves the central hub around that patterns of gene expression are established to specify CZ, PZ, and RM to form a functional SAM.Here, we extend our previous observation of live-imaging to show that the culmination of auxin signaling in PZ is contributed by local auxin biosynthesis besides polar transport, and together they control stem cell differentiation in SAM. To maintain the fate of stem cells, WUS negatively regulates auxin responses in the CZ by directly regulating auxin biosynthesis and signaling genes to counter the differentiation pathways. Furthermore, we show that the enlarged CZ in clv3 mutant plants maintains DII-Venus stably, suggesting that the stem cell fate and auxin signaling are dynamically regulated to maintain the overall SAM organization. Results TAA1 and TAR2 are expressed in shootA previous live-imaging study has shown that transient downregulation of WUS in the stem cell niche results in higher auxin responses in the PZ with ectopic stem cell differentiation,

Auxin and Flower Development: A Blossoming Field

“…Precise spatiotemporal local auxin biosynthesis within the IM and its polar transport and accumulation at specific sites from sources elsewhere in the plant are essential for FM initiation (Alvarez-Buylla et al 2010;Yadav et al 2019). This is evidenced by classical mutants, for example, in PIN-FORMED1 (PIN1), which encodes a polar auxin efflux carrier (Gälweiler et al 1998).…”

Apical and basal auxin sources pattern shoot branching in a moss

“…Although thallus branching occurs by notch dichotomy, a type of apical branching that is developmentally distinct from gametophore branching 7,26 , Marchantia taa and yuc knock-down plants also display hyperbranching phenotypes. Beyond bryophytes, various studies in the flowering plant Arabidopsis thaliana have shown that AtTAA1/WEI8, AtTAR2, AtYUC1 , AtYUC4 and AtYUC6 genes are expressed in discrete and partially overlapping domains of the shoot apical meristem 14,15 . Double and triple mutants in these genes, including yuc1yuc4, yuc1yuc4yuc6 and taa1tar2 allele combinations, show various degrees of decreased apical dominance reflected by an enhanced production of branches.…”

“…Auxin is derived from tryptophan (TRP)-independent and dependent biosynthetic pathways 13 . In the latter, the dominant pathway in plants, TRP is converted to indole-3-pyruvic acid (IPyA) by TRYPTOPHAN AMINO-TRANSFERASE (TAA/TAR) enzymes, that is then converted to auxin by YUCCA FLAVIN MONOOXYGENASE-LIKE (YUC) enzymes [14][15][16][17] . Auxin metabolite profiling in PpTAR and PpYUC overexpression lines, and pptar mutants have suggested that both steps of auxin biosynthesis are essential and identified TRP-to-IPyA conversion as a rate-limiting step in P. patens 13,18,19 .…”

TWISTED DWARF1 regulates Arabidopsis stamen development by differential activation of ABCB-mediated auxin transport

“…Imaging of the synthetic auxin response reporters, DR5::GFP and DII::Venus, at consecutive time points during flower development revealed that auxin response maxima in the floral meristem colocalize with the positions of organ initiation (Goldental-Cohen et al, 2017; van Mourik et al, 2012). Precise spatiotemporal local auxin biosynthesis and its polar transport are essential for floral meristem initiation and subsequent development (Alvarez-Buylla et al, 2010; Yadav et al, 2020).…”