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ABSTRACT: A long-standing question in plants and animals is how spatial patterns are maintained within stem cell niches despite ongoing cell divisions. Here we address how, during shoot meristem formation in Arabidopsis thaliana, the three apical cell layers acquire stem cell identity. Using a sensitized mutant screen, we identified miR394 as a mobile signal produced by the surface cell layer (the protoderm) that confers stem cell competence to the distal meristem by repressing the F box protein LEAF CURLING RESPONSIVENESS. This repression is required to potentiate signaling from underneath the stem cells by the transcription factor WUSCHEL, maintaining stem cell pluripotency. The interaction of two opposing signaling centers provides a mechanistic framework of how stem cells are localized at the tip of the meristem. Although the constituent cells change, the surface layer provides a stable point of reference in the self-organizing meristem.
Developmental cell 01/2013; · 13.36 Impact Factor
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ABSTRACT: During embryogenesis, the basic body plan of an organism develops from a unicellular zygote. In most flowering plants, the polar zygote divides asymmetrically, making visible the apical-basal axis in the early embryo. The molecular mechanisms governing how the zygote polarizes and how this polarity is linked to embryo axis formation have been obscure, mainly owing to the difficulties to access the zygote that is deeply embedded in the maternal tissue. In this review, we summarize recent findings identifying key regulators in Arabidopsis and developing novel approaches in various plant species, which altogether set the stage for unraveling embryo axis formation.
Current opinion in plant biology 08/2012; · 10.33 Impact Factor
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Daoquan Xiang,
Hui Yang,
Prakash Venglat,
Yongguo Cao,
Rui Wen,
Maozhi Ren,
Sandra Stone,
Edwin Wang,
Hong Wang,
Wei Xiao,
Dolf Weijers,
Thomas Berleth, Thomas Laux,
Gopalan Selvaraj,
Raju Datla
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ABSTRACT: The shoot and root apical meristems (SAM and RAM) formed during embryogenesis are crucial for postembryonic plant development. We report the identification of POPCORN (PCN), a gene required for embryo development and meristem organization in Arabidopsis thaliana. Map-based cloning revealed that PCN encodes a WD-40 protein expressed both during embryo development and postembryonically in the SAM and RAM. The two pcn alleles identified in this study are temperature sensitive, showing defective embryo development when grown at 22°C that is rescued when grown at 29°C. In pcn mutants, meristem-specific expression of WUSCHEL (WUS), CLAVATA3, and WUSCHEL-RELATED HOMEOBOX5 is not maintained; SHOOTMERISTEMLESS, BODENLOS (BDL) and MONOPTEROS (MP) are misexpressed. Several findings link PCN to auxin signaling and meristem function: ectopic expression of DR5(rev):green fluorescent protein (GFP), pBDL:BDL-GFP, and pMP:MP-β-glucuronidase in the meristem; altered polarity and expression of pPIN1:PIN1-GFP in the apical domain of the developing embryo; and resistance to auxin in the pcn mutants. The bdl mutation rescued embryo lethality of pcn, suggesting that improper auxin response is involved in pcn defects. Furthermore, WUS, PINFORMED1, PINOID, and TOPLESS are dosage sensitive in pcn, suggesting functional interaction. Together, our results suggest that PCN functions in the auxin pathway, integrating auxin signaling in the organization and maintenance of the SAM and RAM.
The Plant Cell 12/2011; 23(12):4348-67. · 8.99 Impact Factor
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ABSTRACT: Unlike animals, higher plants do not establish a germ line in embryo development but form haploid germ cells from diploid somatic cells late in their life cycle. However, despite its prime importance, little is known about how this transition is regulated.
Here, we show that the WUSCHEL (WUS) gene, initially identified as a stem cell regulator in the shoot meristem, is required for megasporogenesis and thus ultimately for the formation of female generative cells. WUS functions in this process by indirectly activating the expression of the WINDHOSE1 (WIH1) and WIH2 genes that encode small peptides found in plants and fungi, but not in animals. WIH genes function together with the tetraspanin-type protein TORNADO2 (TRN2)/EKEKO in promoting megasporogenesis.
Together, our studies identify a pathway promoting germ cell formation from somatic precursor cells.
Current biology: CB 06/2011; 21(12):1009-17. · 10.99 Impact Factor
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ABSTRACT: Cell-to-cell communication is integral to the evolution of multicellularity. In plant development, peptide signals relay information coordinating cell proliferation and differentiation. These peptides are often encoded by gene families and bind to corresponding families of receptors. The precise spatiotemporal expression of signals and their cognate receptors underlies developmental patterning, and expressional and biochemical changes over evolutionary time have likely contributed to the refinement and complexity of developmental programs. Here, we discuss two major plant peptide families which have central roles in plant development: the CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE) peptide family and the EPIDERMAL PATTERNING FACTOR (EPF) family. We discuss how specialization has enabled the CLE peptides to modulate stem cell differentiation in various tissue types, and how differing activities of EPF peptides precisely regulate the stomatal developmental program, and we examine the contributions of these peptide families to plant development from an evolutionary perspective.
Current biology: CB 05/2011; 21(9):R356-64. · 10.99 Impact Factor
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Developmental cell 03/2011; 20(3):408. · 13.36 Impact Factor
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ABSTRACT: During plant embryogenesis, a simple body plan consisting of shoot and root meristem that are connected by the embryo axis is set up by the first few rounds of cell divisions after fertilization. Postembryonically, the elaborate architecture of plants is created from stem cell populations of both meristems. Here, we address how the main axis (apical-basal) of the plant embryo is established from the single-celled zygote and the role that the asymmetric division of the zygote plays in this process. We will mainly draw on examples from the model plant Arabidopsis, for which several key regulators have been identified during the last years.
Sexual Plant Reproduction 01/2011; 24(2):161-9. · 1.87 Impact Factor
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Jiehua Wang,
Sara Andersson-Gunnerås,
Ioana Gaboreanu,
Magnus Hertzberg,
Matthew R Tucker,
Bo Zheng,
Joanna Leśniewska,
Ewa J Mellerowicz, Thomas Laux,
Göran Sandberg,
Brian Jones
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ABSTRACT: SHORT-ROOT (SHR) is a well characterized regulator of cell division and cell fate determination in the Arabidopsis primary root. However, much less is known about the functions of SHR in the aerial parts of the plant. In this work, we cloned SHR gene from Populus trichocarpa (PtSHR1) as an AtSHR ortholog and down-regulated its expression in hybrid poplar (Populus tremula×P. tremuloides Michx-clone T89) in order to determine its physiological functions in shoot development. Sharing a 90% similarity to AtSHR at amino acid level, PtSHR1 was able to complement the Arabidopsis shr mutant. Down regulation of PtSHR1 led to a strong enhancement of primary (height) and secondary (girth) growth rates in the transgenic poplars. A similar approach in Arabidopsis showed a comparable accelerated growth and development phenotype. Our results suggest that the response to SHR could be dose-dependent and that a partial down-regulation of SHR could lead to enhanced meristem activity and a coordinated acceleration of plant growth in woody species. Therefore, SHR functions in plant growth and development as a regulator of cell division and meristem activity not only in the roots but also in the shoots. Reducing SHR expression in transgenic poplar was shown to lead to significant increases in primary and secondary growth rates. Given the current interest in bioenergy crops, SHR has a broader role as a key regulator of whole plant growth and development and SHR suppression has considerable potential for accelerating biomass accumulation in a variety of species.
PLoS ONE 01/2011; 6(12):e28878. · 4.09 Impact Factor
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ABSTRACT: Maintenance of stem cells in the Arabidopsis thaliana shoot meristem is regulated by signals from the underlying cells of the organizing center, provided through the transcription factor WUSCHEL (WUS). Here, we report the isolation of several independent mutants of MGOUN1 (MGO1) as genetic suppressors of ectopic WUS activity and enhancers of stem cell defects in hypomorphic wus alleles. mgo1 mutants have previously been reported to result in a delayed progression of meristem cells into differentiating organ primordia (Laufs et al., 1998). Genetic analyses indicate that MGO1 functions together with WUS in stem cell maintenance at all stages of shoot and floral meristems. Synergistic interactions of mgo1 with several chromatin mutants suggest that MGO1 affects gene expression together with chromatin remodeling pathways. In addition, the expression states of developmentally regulated genes are randomly switched in mgo1 in a mitotically inheritable way, indicating that MGO1 stabilizes epigenetic states against stochastically occurring changes. Positional cloning revealed that MGO1 encodes a putative type IB topoisomerase, which in animals and yeast has been shown to be required for regulation of DNA coiling during transcription and replication. The specific developmental defects in mgo1 mutants link topoisomerase IB function in Arabidopsis to stable propagation of developmentally regulated gene expression.
The Plant Cell 03/2010; 22(3):716-28. · 8.99 Impact Factor
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Thomas Laux
Seminars in Cell and Developmental Biology 11/2009; 20(9):1082. · 6.65 Impact Factor
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ABSTRACT: The above ground organs of plants are generated by the shoot apical meristem. Cellular characteristics and molecular markers indicate that the shoot meristem is patterned into domains with different functions, with stem cells residing in the outer three cell layers of the central zone of the meristem. The boundaries of the domains are determined by positional signals. Here we will discuss our current understanding of the signaling network involved in determining stem cell fate and in setting the boundaries of the stem cell niche at the plant shoot apex.
Seminars in Cell and Developmental Biology 09/2009; 20(9):1083-8. · 6.65 Impact Factor
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ABSTRACT: The Arabidopsis ARGONAUTE1 (AGO1) and ZWILLE/PINHEAD/AGO10 (ZLL) proteins act in the miRNA and siRNA pathways and are essential for multiple processes in development. Here, we analyze what determines common and specific function of both proteins. Analysis of ago1 mutants with partially compromised AGO1 activity revealed that loss of ZLL function re-establishes both siRNA and miRNA pathways for a subset of AGO1 target genes. Loss of ZLL function in ago1 mutants led to increased AGO1 protein levels, whereas AGO1 mRNA levels were unchanged, implicating ZLL as a negative regulator of AGO1 at the protein level. Since ZLL, unlike AGO1, is not subjected to small RNA-mediated repression itself, this cross regulation has the potential to adjust RNA silencing activity independent of feedback dynamics. Although AGO1 is expressed in a broader pattern than ZLL, expression of AGO1 from the ZLL promoter restored transgene PTGS and most developmental defects of ago1, whereas ZLL rescued only a few AGO1 functions when expressed from the AGO1 promoter, suggesting that the specific functions of AGO1 and ZLL are mainly determined by their protein sequence. Protein domain swapping experiments revealed that the PAZ domain, which in AGO1 is involved in binding small RNAs, is interchangeable between both proteins, suggesting that this common small RNA-binding domain contributes to redundant functions. By contrast, the conserved MID and PIWI domains, which are involved in 5'-end small RNA selectivity and mRNA cleavage, and the non-conserved N-terminal domain, to which no function has been assigned, provide specificity to AGO1 and ZLL protein function.
PLoS Genetics 09/2009; 5(9):e1000646. · 8.69 Impact Factor
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ABSTRACT: The WOX genes form a plant-specific subclade of the eukaryotic homeobox transcription factor superfamily, which is characterized by the presence of a conserved DNA-binding homeodomain. The analysis of WOX gene expression and function shows that WOX family members fulfill specialized functions in key developmental processes in plants, such as embryonic patterning, stem-cell maintenance and organ formation. These functions can be related to either promotion of cell division activity and/or prevention of premature cell differentiation. The phylogenetic tree of the plant WOX proteins can be divided into three clades, termed the WUS, intermediate and ancient clade. WOX proteins of the WUS clade appear to some extent able to functionally complement other members. The specific function of individual WOX-family proteins is most probably determined by their spatiotemporal expression pattern and probably also by their interaction with other proteins, which may repress their transcriptional activity. The prototypic WOX-family member WUS has recently been shown to act as a bifunctional transcription factor, functioning as repressor in stem-cell regulation and as activator in floral patterning. Past research has mainly focused on part of the WOX protein family in some model flowering plants, such as Arabidopsis thaliana (thale cress) or Oryza sativa (rice). Future research, including so-far neglected clades and non-flowering plants, is expected to reveal how these master switches of plant differentiation and embryonic patterning evolved and how they fulfill their function.
Genome biology 01/2009; 10(12):248. · 6.63 Impact Factor
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Franck Anicet Ditengou,
William D Teale,
Philip Kochersperger,
Karl Andreas Flittner,
Irina Kneuper,
Eric van der Graaff,
Hugues Nziengui,
Francesco Pinosa,
Xugang Li,
Roland Nitschke, Thomas Laux,
Klaus Palme
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ABSTRACT: Lateral roots are initiated postembryonically in response to environmental cues, enabling plants to explore efficiently their underground environment. However, the mechanisms by which the environment determines the position of lateral root formation are unknown. In this study, we demonstrate that in Arabidopsis thaliana lateral root initiation can be induced mechanically by either gravitropic curvature or by the transient bending of a root by hand. The plant hormone auxin accumulates at the site of lateral root induction before a primordium starts to form. Here we describe a subcellular relocalization of PIN1, an auxin transport protein, in a single protoxylem cell in response to gravitropic curvature. This relocalization precedes auxin-dependent gene transcription at the site of a new primordium. Auxin-dependent nuclear signaling is necessary for lateral root formation; arf7/19 double knock-out mutants normally form no lateral roots but do so upon bending when the root tip is removed. Signaling through arf7/19 can therefore be bypassed by root bending. These data support a model in which a root-tip-derived signal acts on downstream signaling molecules that specify lateral root identity.
Proceedings of the National Academy of Sciences 12/2008; 105(48):18818-23. · 9.68 Impact Factor
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ABSTRACT: Stem cells are maintained in an undifferentiated state by signals from their microenvironment, the stem cell niche. Despite its central role for organogenesis throughout the plant's life, little is known about how niche development is regulated in the Arabidopsis embryo. Here we show that, in the absence of functional ZWILLE (ZLL), which is a member of the ARGONAUTE (AGO) family, stem cell-specific expression of the signal peptide gene CLAVATA3 (CLV3) is not maintained despite increased levels of the homeodomain transcription factor WUSCHEL (WUS), which is expressed in the organising centre (OC) of the niche and normally promotes stem cell identity. Tissue-specific expression indicates that ZLL acts to maintain the stem cells from the neighbouring vascular primordium, providing direct evidence for a non-cell-autonomous mechanism. Furthermore, mutant and marker gene analyses suggest that during shoot meristem formation, ZLL functions in a similar manner but in a sequential order with its close homologue AGO1, which mediates RNA interference. Thus, WUS-dependent OC signalling to the stem cells is promoted by AGO1 and subsequently maintained by a provascular ZLL-dependent signalling pathway.
Development 09/2008; 135(17):2839-43. · 6.60 Impact Factor
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ABSTRACT: Axis formation is one of the earliest patterning events in plant and animal embryogenesis. In Arabidopsis, the main axis of the embryo is evident at the asymmetric division of the zygote into a small, embryonic apical cell and a large extraembryonic basal cell. Here we show that the homeobox genes WOX2 and WOX8, which are initially coexpressed in the zygote, act as complementary cell fate regulators in the apical and basal lineage, respectively. Furthermore, WOX8 expression in the basal cell lineage is required for WOX2 expression and normal development of the proembryo, suggesting an inductive mechanism. The identified WOX cascade is required for normal expression of a reporter gene of the auxin efflux carrier PIN1 and for the formation of auxin response maxima in the proembryo. Thus, our results link the spatial separation of WOX transcription factors to localized auxin response and the formation of the main body axis in the embryo.
Developmental cell 07/2008; 14(6):867-76. · 13.36 Impact Factor
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ABSTRACT: Polycomb group (PcG) proteins are evolutionary conserved proteins that stably maintain established transcriptional patterns over cell generations. The FERTILIZATION INDEPENDENT SEED (FIS) PcG complex from plants has a similar composition to the Polycomb repressive complex 2 from animals. Mutations in FIS genes cause parent-of-origin-dependent seed abortion. Every seed inheriting a mutant fis allele from the mother is destined to abort, regardless of the presence of a wild-type paternal allele. We tested in Arabidopsis whether the parent-of-origin-dependent seed abortion caused by lack of the FIS subunit MSI1 is caused by parental imprinting of the MSI1 gene. Our data show that MSI1 is not an imprinted gene and that early paternal MSI1 expression is not sufficient to rescue msi1 mutant seeds. By contrast, expression of MSI1 in msi1 female gametophytes is necessary to restore normal seed development, strongly arguing that the female gametophytic effect of fis mutants is caused by a functional requirement for an intact FIS complex in the female gametophyte. Thus, FIS-mediated expression patterns established in the female gametophyte can impact on seed development, establishing fis mutants as true female gametophytic maternal-effect mutants.
Development 11/2007; 134(20):3639-48. · 6.60 Impact Factor
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ABSTRACT: Stem cell niches are specialized microenvironments where pluripotent cells are maintained to provide undifferentiated cells for the formation of new tissues and organs. The balance between stem cell maintenance within the niche and differentiation of cells that exit it is regulated by local cell-cell communication, together with external cues. Recent findings have shown connections between key developmental pathways and added significant insights into the central principles of stem cell maintenance in plant meristems. These insights include the convergence of important stem cell transcriptional regulators with cytokinin signaling in the shoot meristem, the biochemical dissection of peptide signaling in the shoot niche and the identification of conserved regulators in shoot and root niches.
Trends in cell biology 09/2007; 17(8):403-10. · 12.12 Impact Factor
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ABSTRACT: Throughout the lifespan of a plant, which in some cases can last more than one thousand years, the stem cell niches in the root and shoot apical meristems provide cells for the formation of complete root and shoot systems, respectively. Both niches are superficially different and it has remained unclear whether common regulatory mechanisms exist. Here we address whether root and shoot meristems use related factors for stem cell maintenance. In the root niche the quiescent centre cells, surrounded by the stem cells, express the homeobox gene
Nature 04/2007; 446(7137):811-814. · 36.28 Impact Factor
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ABSTRACT: During anther development a series of cell specification events establishes the male gametophyte and the surrounding sporophytic structure. Here we show that the homeobox gene WUSCHEL, originally identified as a central regulator of stem cell maintenance, plays an important role in cell type specification during male organogenesis. WUS expression is initiated very early during anther development in the precursor cells of the stomium and terminates just before the stomium cells enter terminal differentiation. At this stage the stomium cells and the neighboring septum cells that separate the pollen sacs undergo typical cell wall thickening and degenerate which leads to rupture of the anther and pollen release. In wus mutants, neither stomium cells nor septum cells differentiate or undergo cell death and degenerate. As a consequence, the anther stays intact and pollen is not released. CLAVATA3 which is activated by WUS in stem cell maintenance, is not activated in anthers indicating a novel pathway regulated by WUS. Comparing WUS function in stem cell maintenance and sexual organ development suggests that WUS expressing cells represent a conserved signaling module that regulates behavior and communication of undifferentiated cells.
Developmental Biology 03/2007; 302(1):154-9. · 4.07 Impact Factor
