Dynamic and Compensatory Responses of<i>Arabidopsis</i>Shoot and Floral Meristems to<i>CLV3</i>Signaling

Müller, Ralf; Borghi, Loris; Kwiatkowska, Dorota; Laufs, Patrick; Simon, Rüdiger

doi:10.1105/tpc.105.040444

Cited by 156 publications

(156 citation statements)

References 34 publications

(47 reference statements)

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“…5 D and E and Fig. S7 A and B), in agreement with earlier studies (30,31). The ubiquitous overexpression of WUS using a dexamethasone (Dex)-inducible system (35S::eGFP-WUS-GR) also destabilized WUS protein (26).…”

Section: Wus Binds To Cis Elements In a Concentration-dependent Mannersupporting

confidence: 79%

“…The cis element manipulation analysis reveals that WUS activates CLV3 transcription at lower concentrations and represses CLV3 transcription at higher concentrations. Earlier studies have shown that ectopic overexpression of WUS leads to activation of CLV3, a result that is not consistent with higher WUS levels leading to CLV3 repression (30,31). However, these studies only analyzed WUS mRNA patterns and did not analyze WUS protein distribution patterns following ectopic activation.…”

Section: Wus Binds To Cis Elements In a Concentration-dependent Mannermentioning

confidence: 89%

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Threshold-dependent transcriptional discrimination underlies stem cell homeostasis

Perales

Rodriguez

Snipes

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

116

157

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Transcriptional mechanisms that underlie the dose-dependent regulation of gene expression in animal development have been studied extensively. However, the mechanisms of dose-dependent transcriptional regulation in plant development have not been understood. In Arabidopsis shoot apical meristems, WUSCHEL (WUS), a stem cell-promoting transcription factor, accumulates at a higher level in the rib meristem and at a lower level in the central zone where it activates its own negative regulator, CLAVATA3 (CLV3). How WUS regulates CLV3 levels has not been understood. Here we show that WUS binds a group of cis-elements, cis-regulatory module, in the CLV3-regulatory region, with different affinities and conformations, consisting of monomers at lower concentration and as dimers at a higher level. By deleting cis elements, manipulating the WUSbinding affinity and the homodimerization threshold of cis elements, and manipulating WUS levels, we show that the same cis elements mediate both the activation and repression of CLV3 at lower and higher WUS levels, respectively. The concentrationdependent transcriptional discrimination provides a mechanistic framework to explain the regulation of CLV3 levels that is critical for stem cell homeostasis.WUSCHEL | cis-regulatory module | CLAVATA3 | shoot apical meristem | gene regulation

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Section: Wus Binds To Cis Elements In a Concentration-dependent Mannersupporting

confidence: 79%

Section: Wus Binds To Cis Elements In a Concentration-dependent Mannermentioning

confidence: 89%

Threshold-dependent transcriptional discrimination underlies stem cell homeostasis

Perales

Rodriguez

Snipes

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

116

157

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“…It is possible that CLV3 expression in L1, which persists during RBR downregulation, is sufficient to reestablish the meristem by resetting the CLV/WUS feedback loop, which is known to be robust and flexible (Muller et al, 2006). About 30% of the arrested meristems recovered a twin stem cell domain, similar to meristems in which the central zone was ablated (Reinhardt et al, 2003).…”

Section: Rbr Homeostasis Is Critical For Meristem Integrity and Functionmentioning

confidence: 98%

ArabidopsisRETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production

et al. 2010

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Several genes involved in the regulation of postembryonic organ initiation and growth have been identified. However, it remains largely unclear how developmental cues connect to the cell cycle. RETINOBLASTOMA RELATED (RBR) is a plant homolog of the tumor suppressor Retinoblastoma (pRb), which is a key regulator of the cell cycle. Using inducible RNA interference (RNAi) against Arabidopsis thaliana RBR (RBRi), we reduced RBR expression levels at different stages of plant development. Conditional reduction or loss of RBR function disrupted cell division patterns, promoted context-dependent cell proliferation, and negatively influenced establishment of cell differentiation. Several lineages of toti-and pluripotent cells, including shoot apical meristem stem cells, meristemoid mother cells, and procambial cells, failed to produce appropriately differentiated cells. Meristem activity was altered, leading to a disruption of the CLAVATA-WUSCHEL feedback loop and inhibition of lateral organ formation. Release of RBR from RNAi downregulation restored meristem activity. Gene profiling analyses soon after RBRi induction revealed that a change in RBR homeostasis is perceived as a stress, even before genes regulated by RBR-E2F become deregulated. The results establish RBR as a key cell cycle regulator required for coordination of cell division, differentiation, and cell homeostasis. INTRODUCTIONRetinoblastoma (RB) was the first tumor suppressor gene identified in animals (Friend et al., 1986) and later was associated with cell cycle regulation, thus establishing pRb as a key regulator of cell proliferation. In animals, three members of the RB family of proteins (pRb, p107, and p130), also referred to as pocket proteins (Mulligan and Jacks, 1998), negatively regulate the G1-to-S phase transition during the cell cycle. It is now widely accepted that mitogenic signals activate several cyclin-dependent kinase (CDK)-cyclin complexes during progression through G1 to phosphorylate pRb, thereby releasing it from interactions with E2F/DP transcription factor complexes to facilitate S-phase entry (Weinberg, 1995). Subsequently, pRb was also found to regulate tissue-specific transcription factors that regulate cell differentiation, such as MyoD, which activates muscle-specific genes (De Falco et al., 2006). pRb also regulates germ cell proliferation, differentiation, and survival (Toppari et al., 2003) and is required for osteoblast, keratinocyte, and macrophage differentiation (Nead et al., 1998;Liu et al., 1999;Thomas et al., 2003). Together with the tumor suppressor p53, pRb regulates adipocyte differentiation and function (Hallenborg et al., 2009). The requirement for RB in cell differentiation therefore extends beyond regulation of cell cycle entry. For example, the loss of RB function in cardioblasts affects cell differentiation by modulating the activity of cardiogenic factors (Papadimou et al., 2005).RB-related genes, termed RETINOBLASTOMA-RELATED (RBR; Ach et al., 1997), are also found in monocots (Grafi et al., 1996;Xie et al...

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“…The CLE44-overexpressing plants showed bushy-like appearance (data not shown). the CLV3 receptor CLV1 is an LRR-RLK (1,(5)(6)(7)(8)(9), by analogy we expected that a receptor for TDIF might also be an LRR-RLK or an LRR-RLP. In the Arabidopsis genome, more than 200 LRR-RLK and more than 50 LRR-RLP genes have been annotated (22).…”

Section: Tdif Promotes Procambial Cell Proliferation While Suppressinmentioning

confidence: 99%

“…The fate of stem cells in the SAM and the RAM is controlled by the transcription factors WUSCHEL (WUS) (2) and WUSCHELrelated homeobox 5 (WOX5) (3), respectively. In SAM, the expression of WUS is regulated by the CLAVATA (CLV) system involving CLV3, a member of the CLV3/ESR-related (CLE) family and the CLV1 (LRR-LRK)/CLV2 (a leucine-rich repeat receptor-like protein, LRR-RLP) complex (4)(5)(6)(7)(8)(9). In the vascular meristem, a few layers of stem cells proliferate, and their progeny differentiate into apposing xylem and phloem cells (10,11).…”

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confidence: 99%

Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system

Hirakawa

Shinohara

Kondo

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

454

555

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Land plants evolved a long-distance transport system of water and nutrients composed of the xylem and phloem, both of which are generated from the procambium-and cambium-comprising vascular stem cells. However, little is known about the molecular mechanism of cell communication governing xylem-phloem patterning. Here, we show that a dodecapeptide (HEVHypSGHypN-PISN; Hyp, 4-hydroxyproline), TDIF (tracheary element differentiation inhibitory factor), is secreted from the phloem and suppresses the differentiation of vascular stem cells into xylem cells through a leucine-rich repeat receptor-like kinase (LRR-RLK). TDIF binds in vitro specifically to the LRR-RLK, designated TDR (putative TDIF receptor), whose expression is restricted to procambial cells. However, the combined analysis of TDIF with a specific antibody and the expression profiles of the promoters of two genes encoding TDIF revealed that TDIF is synthesized mainly in, and secreted from, the phloem and its neighboring cells. The observation that TDIF is capable of promoting proliferation of procambial cells while suppressing xylem differentiation suggests that this small peptide functions as a phloem-derived, non-cellautonomous signal that controls stem cell fate in the procambium. Our results indicate that we have discovered a cell communication system governing phloem-xylem cross-talk.CLV3/ESR-related (CLE) ͉ leucine-rich repeat receptor-like kinase ͉ phloem ͉ procambium ͉ xylem

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Dynamic and Compensatory Responses ofArabidopsisShoot and Floral Meristems toCLV3Signaling

Cited by 156 publications

References 34 publications

Threshold-dependent transcriptional discrimination underlies stem cell homeostasis

Threshold-dependent transcriptional discrimination underlies stem cell homeostasis

ArabidopsisRETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production

Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system

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