Plant Stem Cells Research Articles

Hypersensitivity to DNA damage in plant stem cell niches

The growing apices of plants contain stem cells that continually produce tissues, which, in the shoot, include the germline. These stem cell populations remain active throughout the plant's life, which can last for centuries, and are particularly exposed to environmental hazards that cause DNA damage and mutations. It is not known whether plants have mechanisms to safeguard the genome specifically in these crucial cell populations. Here, we show that root and shoot stem cells and their early descendants are selectively killed by mild treatment with radiomimetic drugs, x-rays, or mutations that disrupt DNA repair by nonhomologous end-joining. Stem cell death required transduction of DNA damage signals by the ATAXIA-TELANGIECTASIA MUTATED (ATM) kinase and, specifically in the root, also the ATM/RAD3-RELATED (ATR) kinase. Consistent with the absence of p53 and the core apoptotic machinery in plants, death of the stem cells did not show apoptotic but autolytic features as seen in other cases of plant developmentally programmed cell death. We propose that plants have independently evolved selective death as a stringent mechanism to safeguard genome integrity in their stem cell populations.

Cytokinin and WUSCHEL tie the knot around plant stem cells

Once upon a time, plant development was all about hormones. Darwin (1) wrote nearly 130 years ago that “some influence,” later shown to be the phytohormone auxin, moved down the shoot to control the elongation of oat seedlings. In the 1950s, Skoog and Miller (2) showed that auxin and cytokinin control shoot regeneration in vitro, a technique that is extensively used to this day. With the rise of developmental genetics at the end of the 20th century, however, plant development became focused on transcription factors and their exquisite expression patterns. More recently, both views have converged to explain how plants develop intricate structures with precise expression patterns superimposed on cells that are constantly displaced by growth. This convergence was first exemplified by the role of auxin in patterning the growing root tip (3). In this issue of PNAS, Gordon et al. (4) shed light on the interplay of regulatory genes and cytokinin in the dynamic patterning of the opposite end of the plant, the shoot meristem.

A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem

Developmental regulation of the floral meristem ensures that plants of the same species have similarly sized flowers with a fixed number of floral organs. The maintenance of stem cells in the floral meristem is terminated after the production of a fixed number of floral organ primordia. Precise repression of the Arabidopsis thaliana homeobox gene WUSCHEL (WUS) by the floral homeotic protein AGAMOUS (AG) plays a major part in this process. Here we show that KNUCKLES (KNU) mediates the repression of WUS in floral meristem determinacy control. AG directly induces the transcription of KNU, which encodes a C2H2-type zinc finger protein with a conserved transcriptional repression motif. In turn, KNU represses WUS transcription to abolish stem cell activity. We also show that the timing of KNU induction is key in balancing proliferation and differentiation in flower development. Delayed KNU expression results in an indeterminate meristem, whereas ectopic KNU expression prematurely terminates the floral meristem. Furthermore, KNU induction by AG is preceded by changes in repressive histone modification at the KNU locus, which occurs in an AG-dependent manner. This study provides a mechanistic link between transcriptional feedback and epigenetic regulation in plant stem cell proliferation.

Plant stem cells, not so different

New technique allows gene-expression analysis

A Quantitative and Dynamic Model for Plant Stem Cell Regulation

Plants maintain pools of totipotent stem cells throughout their entire life. These stem cells are embedded within specialized tissues called meristems, which form the growing points of the organism. The shoot apical meristem of the reference plant Arabidopsis thaliana is subdivided into several distinct domains, which execute diverse biological functions, such as tissue organization, cell-proliferation and differentiation. The number of cells required for growth and organ formation changes over the course of a plants life, while the structure of the meristem remains remarkably constant. Thus, regulatory systems must be in place, which allow for an adaptation of cell proliferation within the shoot apical meristem, while maintaining the organization at the tissue level. To advance our understanding of this dynamic tissue behavior, we measured domain sizes as well as cell division rates of the shoot apical meristem under various environmental conditions, which cause adaptations in meristem size. Based on our results we developed a mathematical model to explain the observed changes by a cell pool size dependent regulation of cell proliferation and differentiation, which is able to correctly predict CLV3 and WUS over-expression phenotypes. While the model shows stem cell homeostasis under constant growth conditions, it predicts a variation in stem cell number under changing conditions. Consistent with our experimental data this behavior is correlated with variations in cell proliferation. Therefore, we investigate different signaling mechanisms, which could stabilize stem cell number despite variations in cell proliferation. Our results shed light onto the dynamic constraints of stem cell pool maintenance in the shoot apical meristem of Arabidopsis in different environmental conditions and developmental states.

Pattern formation by small RNA signals

Plant stem cells not only serve as a persistent source of cells from which lateral organs arise, they also produce signals important for the patterning of lateral organs. Our work focuses on small regulatory RNAs as potential signals. Leaves of higher plants exhibit a varying degree of asymmetry along their dorsoventral axis. This asymmetry is specified via the polarized expression of class III homeodomain-leucine zipper (hd-zipIII) genes, which specify dorsal cell fate. Through detailed in situ hybridization analyses we were able to show that this polarized hd-zipIII expression is set up by the graded expression pattern of a 21-nucleotide microRNA, miR166. More recently, we have shown that this miR166 gradient is generated through the opposing activity of a different small regulatory RNA, the transacting siRNA tasiR-ARF. A further twist to the story is added by the observation that tasiR-ARF in turn is regulated by a third small RNA, miR390. Our observations identify a novel mechanism of pattern formation in which cell fates along a developmental axis are specified through the opposing activities of distinct small RNAs. miR390 and tasiR-ARF define the dorsal side of the leaf by restricting the expression domain of miR166, which in turn delineates the ventral side by restricting expression of the HD-ZIPIII transcription factors. Importantly, comparison of the expression patterns of small RNA precursor transcripts to those of the mature small RNAs provides evidence that small regulatory RNAs may traffic between cells, which offers the intriguing possibility that small RNAs may function as mobile signals in development.

Plant Stem Cell Niches: Standing the Test of Time

Similar to animal stem cells, plant stem cells require special niche microenvironments to continuously generate the tissues that constitute the plant body. Recent work using computer modeling and live imaging is helping to elucidate some of the mechanisms responsible for the specification and maintenance of stem cells in the root and shoot.

Stem cells in the root and the problem of stem cells in plants

Plant cells are capable of reversible transition from the proliferating to the stem state. This transition is determined by a system of cell-cell interactions and interrelationships between plant parts. Stem cells defined as the cells preserving the capacity to divisions and differentiation for a long time arise repeatedly during development of the root and shoot primordial, rather than are clones of a population of stem cells laid down at a certain stage of embryogenesis. The quiescent center cells, rather than the surrounding actively dividing cells, best correspond to the characteristics of stem cells according to Loeffler and Potten. The factors that determine the quiescent center formation and maintenance in the root have been analyzed. The available data suggest that among these factors, indoleacetic acid transport and cap influence are of paramount significance. The cap formation precedes the quiescent center formation both during the root development and in the course of meristem regeneration after the root decapitation. The capacity of tem cell formation by the meristem suggests that not only meristem arises from the stem cells, but also that stem cells are formed from actively dividing cells. Repeated formation of stem cells allows long-term preservation of the capacity of plants for open morphogenesis and vegetative propagation.

The germ track and stem cells in higher plants

A. Weisman’s conception of the germ track is considered within a historical context and the fundamental distinctions in the methods of forming the germ track cells in animals and plants are underscored. In animals differentiation of germ track cells is realized once at the start of embryogenesis, whereas in higher plants this process is achieved repeatedly throughout the entire life of the plant. Fundamental differences in morpho-and embryogenesis in animals and plants as well as differences in the properties of somatic and germ cells provide plants with special paths of hereditary variability and evolution which are not present in animals.

The dynamic plant stem cell niches

Stem cells exist in specific locations called niches, where extracellular signals maintain stem cell division and prevent differentiation. In plants, the best characterised niches are within the shoot and root meristems. Networks of regulatory genes and intercellular signals maintain meristem structure in spite of constant cell displacement by division. Recent works have improved our understanding of how these networks function at the cellular and molecular levels, particularly in the control of the stem cell population in the shoot meristem. The meristem regulatory genes have been found to function partly through localised control of widely used signals such as cytokinin and auxin. The retinoblastoma protein has also emerged as a key regulator of cell differentiation in the meristems.

Pluripotent versus totipotent plant stem cells: dependence versus autonomy?

Little is known of the mechanisms that induce the dedifferentiation of a single somatic cell into a totipotent embryogenic cell that can either be regenerated or develop into an embryo and subsequently an entire plant. In this Opinion article, we examine the cellular, physiological and molecular similarities and differences between different plant stem cell types. We propose to extend the plant stem cell concept to include single embryogenic cells as a totipotent stem cell based on their capacity to regenerate or develop into an embryo under certain conditions. Our survey suggests that differences in chromatin structure might ensure that meristem-localized stem cells have supervised freedom and are pluripotent, and that embryogenic stem cells are unsupervised, autonomous and, hence, freely totipotent.

Plant stem cells for the production of pharmaceutical active compounds

Plant stem cells for the production of pharmaceutical active compounds

Peptide Regulators of Plant Development

Cell-cell communication is essential for organized tissue formation. Recently, a role for peptides in plant development has been established. In the shoot apical meristem of Arabidopsis , cell fate determination involves the CLAVATA3 gene, which encodes a putative peptide ligand, and the CLAVATA1 gene, which encodes a leucine-rich repeat receptor-like kinase. However, the precise identity of the individual signaling peptide has remained elusive (see the Perspective by Simon and Stahl). Two independent groups, Ito et al. and Kondo et al. , have now isolated specific CLAVATA-derived 12-amino acid peptides involved in the regulation of plant meristem development. R. Simon, Y. Stahl, Plant cells CLEave their way to differentiation. Science 313 , 773-774 (2006). [Summary] [Full Text] Y. Ito, I. Nakanomyo, H. Motose, K. Iwamoto, S. Sawa, N. Dohmae, H. Fukuda, Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313 , 842-845 (2006). [Abstract] [Full Text] T. Kondo, S. Sawa, A. Kinoshita, S. Mizuno, T. Kakimoto, H. Fukuda, Y. Sakagami, A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313 , 845-848 (2006). [Abstract] [Full Text]

Dodeca-CLE Peptides as Suppressors of Plant Stem Cell Differentiation

In plants and animals, small peptide ligands that signal in cell-cell communication have been suggested to be a crucial component of development. A bioassay of single-cell transdifferentation demonstrates that a dodecapeptide with two hydroxyproline residues is the functional product of genes from the CLE family, which includes CLAVATA3 in Arabidopsis. The dodecapeptide suppresses xylem cell development at a concentration of 10(-11) M and promotes cell division. An application, corresponding to all 26 Arabidopsis CLE protein family members, of synthetic dodecapeptides reveals two counteracting signaling pathways involved in stem cell fate.

MicroRNA regulation of plant stem cell populations

MicroRNA regulation of plant stem cell populations

KNOX Gene Function in Plant Stem Cell Niches

Homeobox genes encode transcriptional regulators that control development in multicellular eukaryotes. In plants, post-embryonic shoot growth relies on the activity of indeterminate cell populations termed shoot meristems, within which members of the class-1 KNOX sub-family of homeobox genes are expressed. KNOX genes are differentially required for meristem development and function to inhibit cell expansion and differentiation associated with organogenesis. Mechanisms must therefore be employed to prevent KNOX gene expression in developing lateral organs such as leaves. This review focuses on the expression patterns, meristematic functions and regulation of KNOX genes, and how the activities of these genes are integrated within the framework of pathways that control plant development.

P. patens protoplast asymmetric cell division : from cell polarity to cell fate determination in plant stem cells

P. patens protoplast asymmetric cell division : from cell polarity to cell fate determination in plant stem cells

Plant stem cell niches

Stem cells are required to support the indeterminate growth style of plants. Meristems are a plants stem cell niches that foster stem cell survival and the production of descendants destined for differentiation. In shoot meristems, stem cell fate is decided at the populational level. The size of the stem cell domain at the meristem tip depends on signals that are exchanged with cells of the organizing centre underneath. In root meristems, individual stem cells are controlled by direct interaction with cells of the quiescent centre that lie in the immediate neighbourhood. Analysis of the interactions and signaling processes in the stem cell niches has delivered some insights into the molecules that are involved and revealed that the two major niches for plant stem cells are more similar than anticipated.

Apical meristems: the plant's fountain of youth.

During postembryonic development, all organs of a plant are ultimately derived from a few pluripotent stem cells found in specialized structures called apical meristems. Here we discuss our current knowledge about the regulation of plant stem cells and their environments with main emphasis on the shoot apical meristem of Arabidopsis thaliana. Recent studies suggest that stem cells are localized in specialized niches where signals from surrounding cells maintain their undifferentiated state. In the shoot meristem, initiation of stem cells during embryogenesis, regulation of stem-cell homeostasis and termination of stem-cell maintenance during flower development appear to primarily involve regulation of the stem-cell niche.

Stem cell regulation in the shoot meristem.

A small group of pluripotent stem cells in the shoot meristem is the ultimate source for all aerial parts in higher plants: the shoot axis, side branches, leaves and flowers. The stem cells are maintained in an undifferentiated state by signals from an underlying cell group, the organizing center. Genetic and molecular analyses have shown that a feedback signaling loop between stem cells and the organizing center balances stem cell renewal versus differentiation, which allows the plant to maintain the organization of the shoot meristem despite a changing cellular context. Emerging common principles indicate that plant and animal stem cells are functionally equivalent.