Feedback from Lateral Organs Controls Shoot Apical Meristem Growth by Modulating Auxin Transport

Kumar

2019

Preprint

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,

Section: Auxin Levels Dynamically Regulate Stem Cell Fate In Samsupporting

confidence: 92%

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

Kumar

2019

Preprint

“…Because MP was also strongly expressed in the PZ (Supplemental Figure 5), we speculated that MP might be involved in the negative control of WUS in the PZ. Support for this idea was derived from the observation that auxin levels are low in the OC and auxin flow from lateral organs negatively regulates SAM size, which is independent of CLV signaling (Shi et al, 2018). Likewise, in auxin-deficient yuc1 yuc2 yuc4 yuc6 mutants, although DRN ( Figure 7B) and CLV3 (Zhao et al, 2010) expression levels were high, the SAM in this quadruple mutant remained enlarged (Supplemental Figure 16G) (Shi et al, 2018).…”

Section: Mp-mediated Auxin Signaling Controls Plant Shoot Stem Cell Hmentioning

confidence: 91%

A Molecular Framework for Auxin-Controlled Homeostasis of Shoot Stem Cells in Arabidopsis

Luo

Zeng

et al. 2018

Molecular Plant

The classic phytohormone auxin plays an essential role in priming meristematic cell differentiation in the shoot apical meristem to promote lateral organ initiation. Recently, several lines of evidence have suggested that auxin is not only transported to new primordia but also descends to the stem cells in the central zone. However, the function of auxin in stem cell regulation has remained elusive. Here, we show that auxin signaling in stem cells is mediated, at least in part, by AUXIN RESPONSE FACTOR 5/MONOPTEROS (ARF5/MP), which directly represses the transcription of DORNROSCHEN/ENHANCER OF SHOOT REGENERATION 1 (DRN/ESR1). DRN expressed in stem cells positively regulates CLAVATA3 (CLV3) expression and has important meristematic functions. Our results provide a mechanistic framework for auxin control of shoot stem cell homeostasis and demonstrate how auxin differentially controls plant stem cell maintenance and differentiation.

“…In maize, a CLAVATA3/ESR-related (CLE) peptide expressed in organ primordia signals to FASCIATED EAR3 (FEA3), a leucinerich-repeat receptor expressed in the SAM, to limit the stem cell population and SAM size (Je et al, 2016). In Arabidopsis, lateral organs feedback on SAM size via modulation of auxin transport (Shi et al, 2018).…”

Section: Acquisition Of a Lateral Organ Fatementioning

confidence: 99%

Getting leaves into shape: a molecular, cellular, environmental and evolutionary view

Maugarny-Calès

Laufs

2018

Development

Leaves arise from groups of undifferentiated cells as small primordia that go through overlapping phases of morphogenesis, growth and differentiation. These phases are genetically controlled and modulated by environmental cues to generate a stereotyped, yet plastic, mature organ. Over the past couple of decades, studies have revealed that hormonal signals, transcription factors and miRNAs play major roles during leaf development, and more recent findings have highlighted the contribution of mechanical signals to leaf growth. In this Review, we discuss how modulating the activity of some of these regulators can generate diverse leaf shapes during development, in response to a varying environment, or between species during evolution.