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PubMed2006

The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution.

In Arabidopsis, stem cell homeostasis in the shoot apical meristem (SAM) is controlled by a feedback loop between WUS and CLV functions. We have identified WUS orthologues in maize and rice by a detailed phylogenetic analysis of the WOX gene family and subsequent cloning. A single WUS orthologue is present in the rice genome (OsWUS), whereas the allotetraploid maize genome contains 2 WUS paralogues (ZmWUS1 and ZmWUS2). None of the isolated grass WUS orthologues displays an organizing center-type expression pattern in the vegetative SAM as in Arabidopsis. In contrast, the grass-specific expression patterns relate to the specification of new phytomers consistent with the transcriptional expression patterns of TD1 and FON1 (CLV1 orthologues of maize and rice, respectively). Moreover, the grass WUS and CLV1 orthologues are coexpressed in all reproductive meristems, where fasciation and supernumerary floral organs occur in td1 or fon1 loss-of-function mutants. The expression patterns of WUS orthologues in both grass species compared with those of dicots imply that major changes in WUS function, which are correlated with changes in CLV1 signaling, have occurred during angiosperm evolution and raise doubts about the uniqueness of the WUS/CLV antagonism in the maintenance of the shoot stem cell niche in grasses.

Amino Acid Sequence↗

PubMed2004

DNA repair in higher plants; photoreactivation is the major DNA repair pathway in non-proliferating cells while excision repair (nucleotide excision repair and base excision repair) is active in proliferating cells.

We investigated expression patterns of DNA repair genes such as the CPD photolyase, UV-DDB1, CSB, PCNA, RPA32 and FEN-1 genes by northern hybridization analysis and in situ hybridization using a higher plant, rice (Oryza sativa L. cv. Nipponbare). We found that all the genes tested were expressed in tissues rich in proliferating cells, but only CPD photolyase was expressed in non-proliferating tissue such as the mature leaves and elongation zone of root. The removal of DNA damage, cyclobutane pyrimidine dimers and (6-4) photoproducts, in both mature leaves and the root apical meristem (RAM) was observed after UV irradiation under light. In the dark, DNA damage in mature leaves was not repaired efficiently, but that in the RAM was removed rapidly. Using a rice 22K custom oligo DNA microarray, we compared global gene expression patterns in the shoot apical meristem (SAM) and mature leaves. Most of the excision repair genes were more strongly expressed in SAM. These results suggested that photoreactivation is the major DNA repair pathway for the major UV-induced damage in non-proliferating cells, while both photoreactivation and excision repair are active in proliferating cells.

Cell Division↗

PubMed2000

Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana.

When mutations in CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 are combined, severe defects involving fusion of sepals and of stamens occur in Arabidopsis flowers. In addition, septa of gynoecia do not fuse along the length of the ovaries and many ovules have their growth arrested. CUC2 is expressed at the tips of septal primordia during gynoecium development and at the boundary between nucellus and chalaza during ovule development. These expression patterns are partially consistent with the phenotype of the mutant gynoecium. CUC2 mRNA is also shown to be expressed at the boundaries between meristems and organ primordia during both the vegetative and reproductive phases. This expression pattern indicates that CUC2 is generally involved in organ separation in shoot and floral meristems.

Arabidopsis↗

PubMed2001

The regulation of ornithine decarboxylase gene expression by sucrose and small upstream open reading frame in tomato (Lycopersicon esculentum Mill).

We identified a near-full-length cDNA clone encoding ornithine decarboxylase (ODC) from tomato (Lycopersicon esculentum Mill). It contained a small upstream open reading frame (uORF) within its 5' untranslated region. An in vitro translation assay demonstrated that the uORF repressed expression of downstream ORF. Neither nucleotide nor predicted peptide sequence of the uORF was responsible for the repression. The presence of upstream AUG codon was shown to be responsible. ODC expression appeared to be organ specific. The ODC gene was expressed in roots, hypocotyls and sink leaves but not in source leaves. ODC transcripts were observed in apical meristem of primary roots, and were distributed in cells of cortex layer preferentially. ODC expression responded immediately to sucrose availability via the sucrose-specific pathway independent of hexokinase. Sucrose induction of ODC gene was seen in roots, hypocotyls and flowers but not in mature leaves. Moreover, only the root apical meristem responded to sucrose availability. These observations indicate that the spatial pattern of ODC expression is closely associated with cell proliferation and that sucrose sensing plays a major role in the spatial pattern of ODC expression. Also, the differential regulation of ODC and arginine decarboxylase gene expression by factors modulating plant growth suggests that they would have different physiological roles in plant development.

5' Untranslated Regions↗

PubMed2006

Oncogene 6b from Agrobacterium tumefaciens induces abaxial cell division at late stages of leaf development and modifies vascular development in petioles.

The 6b gene in the T-DNA region of the Ti plasmids of Agrobacterium tumefaciens and A. vitis is able to generate shooty calli in phytohormone-free culture of leaf sections of tobacco transformed with 6b. In the present study, we report characteristic morphological abnormalities of the leaves of transgenic tobacco and Arabidopsis that express 6b from pTiAKE10 (AK-6b), and altered expression of genes related to cell division and meristem formation in the transgenic plants. Cotyledons and leaves of both transgenic tobacco and Arabidopsis exhibited various abnormalities including upward curling of leaf blades, and transgenic tobacco leaves produced leaf-like outgrowths from the abaxial side. Transcripts of some class 1 KNOX homeobox genes, which are thought to be related to meristem functions, and cell cycle regulating genes were ectopically accumulated in mature leaves. M phase-specific genes were also ectopically expressed at the abaxial sides of mature leaves. These results suggest that the AK-6b gene stimulates the cellular potential for division and meristematic functions preferentially in the abaxial side of leaves and that the leaf phenotypes generated by AK-6b are at least in part due to such biased cell division during polar development of leaves. The results of the present experiments with a fusion gene between the AK-6b gene and the glucocorticoid receptor gene showed that nuclear import of the AK-6b protein was essential for upward curling of leaves and hormone-free callus formation, suggesting a role for AK-6b in nuclear events.

Agrobacterium tumefaciens↗

PubMed2006

Variations in sucrose and ABA concentrations are concomitant with heteroblastic leaf shape changes in a rhythmically growing species (Quercus robur).

In rhythmically growing woody species such as common oak (Quercus robur L.), stem growth is discontinuous and a bud forms at regular intervals at the shoot apex. These buds are composed of different types of leaves: laminate, aborted lamina and scale. The change in heteroblastic leaf shape from laminate to aborted lamina leaves is regarded as one of the events marking shoot growth arrest. To better understand the determinism of heteroblastic leaf shape change and thus, of rhythmicity, we studied morphogenetic events during the early days of the second flush of growth in oak, as well as changes in sucrose metabolism and abscisic acid (ABA) concentrations in control plants expressing the heteroblastic leaf shape change and in defoliated plants showing no heteroblastic leaf shape change and producing only laminate leaves. In control plants, the leaf shape change was underway on Day 5 of the second flush with the differentiation of the first two aborted lamina leaves. Sucrose concentration in the apices of control plants decreased between Days 3 and 5 during differentiation of the aborted lamina leaves. An inverse pattern was observed in defoliated plants, suggesting that sucrose acts as a signal triggering heteroblastic leaf shape changes. During the same period, acid cell wall invertase activity was high in young stem and laminate leaves of control plants, whereas the activity remained constant and low in the apices. If the laminate leaves were removed, the increase in apical sucrose concentration was proportionally higher than the decrease in apical acid vacuolar invertase activity, suggesting that, in the absence of young leaves, sucrose is imported to the apex. The sucrose concentration in the apex is therefore likely to be affected by trophic competition with the expanding laminate leaves. The decrease in apex sucrose concentration may be one of the mechanisms driving heteroblastic leaf shape change. Differentiation of aborted lamina leaves was followed by a decrease in the organogenic activity of the shoot apical meristem (SAM) between Days 7 and 9. High concentrations of ABA are associated with differentiation of aborted lamina and scale leaves and with low SAM organogenic activity. Shoot apical meristem organogenic activity remained high and ABA concentration in the apex remained low in defoliated plants producing only photosynthetic leaves. These results suggest that (1) ABA is involved in the gradual conversion of embryonic leaves to abnormal leaves, thereby regulating heteroblastic leaf shape changes and (2) changes in ABA concentration influence the intensity of SAM organogenic activity. Heteroblastic development and therefore rhythmic growth could be the result of competition between apices and laminate leaves, with competition first involving sucrose and thereafter ABA.

Abscisic Acid↗

PubMed1995

Pattern formation in the Arabidopsis embryo: a genetic perspective.

During embryogenesis, a single cell gives rise to different cell types, tissues and organs which are arranged in a biologically meaningful context, or pattern. The resulting basic body organization of higher plants, which is expressed in the seedling, provides a reference system for postembryonic development during which the meristems of the shoot and the root produce the adult body. The seedling may be viewed as the superimposition of two patterns: one along the apical-basal axis of polarity and the other perpendicular to the axis. To analyse mechanisms underlying pattern formation in the embryo, a genetic approach has been taken in Arabidopsis. Mutations in a small number of genes alter one or the other of the two patterns. The mutant phenotypes suggest that early partitioning of the axis is followed by region-specific development, including the formation of the primary shoot and root meristems. The cloning of two genes involved in pattern formation provides a basis for mechanistic studies of how cells adopt specific fates in the developing embryo.

Arabidopsis↗

PubMed2004

Between the sheets: inter-cell-layer communication in plant development.

The cells of plant meristems and embryos are arranged in an organized, and sometimes extremely beautiful, layered pattern. This pattern is maintained by the controlled orientation of cell divisions within layers. However, despite this layered structure, cell behaviour during plant development is not lineage dependent, and does not occur in a mosaic fashion. Many studies, both classical and recent, have shown that plant cell identity can be re-specified according to position, allowing plants to show remarkable developmental plasticity. However, the layered structure of meristems and the implications of this during plant development, remain subjects of some speculation. Of particular interest is the question of how cell layers communicate, and how communication between cell layers could allow coordinated developmental processes to take place. Recent research has uncovered several examples both of the molecular mechanisms by which cell layers can communicate, and of how this communication can infringe on developmental processes. A range of examples is used to illustrate the diversity of mechanisms potentially implicated in cell-layer communication during plant development.

Cell Communication↗

PubMed2006

Gene discovery and annotation using LCM-454 transcriptome sequencing.

454 DNA sequencing technology achieves significant throughput relative to traditional approaches. More than 261,000 ESTs were generated by 454 Life Sciences from cDNA isolated using laser capture microdissection (LCM) from the developmentally important shoot apical meristem (SAM) of maize (Zea mays L.). This single sequencing run annotated >25,000 maize genomic sequences and also captured approximately 400 expressed transcripts for which homologous sequences have not yet been identified in other species. Approximately 70% of the ESTs generated in this study had not been captured during a previous EST project conducted using a cDNA library constructed from hand-dissected apex tissue that is highly enriched for SAMs. In addition, at least 30% of the 454-ESTs do not align to any of the approximately 648,000 extant maize ESTs using conservative alignment criteria. These results indicate that the combination of LCM and the deep sequencing possible with 454 technology enriches for SAM transcripts not present in current EST collections. RT-PCR was used to validate the expression of 27 genes whose expression had been detected in the SAM via LCM-454 technology, but that lacked orthologs in GenBank. Significantly, transcripts from approximately 74% (20/27) of these validated SAM-expressed "orphans" were not detected in meristem-rich immature ears. We conclude that the coupling of LCM and 454 sequencing technologies facilitates the discovery of rare, possibly cell-type-specific transcripts.

Base Sequence↗

PubMed2004

The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells.

Plant infections by the soil bacterium Agrobacterium rhizogenes result in neoplastic disease with the formation of hairy roots at the site of infection. Expression of a set of oncogenes residing on the stably integrated T-DNA is responsible for the disease symptoms. Besides the rol (root locus) genes, which are essential for the formation of hairy roots, the open reading frame orf13 mediates cytokinin-like effects, suggesting an interaction with hormone signaling pathways. Here we show that ORF13 induced ectopic expression of KNOX (KNOTTED1-like homeobox) class transcription factors, as well as of several genes involved in cell cycle control in tomato (Lycopersicon esculentum). ORF13 has a retinoblastoma (RB)-binding motif and interacted with maize (Zea mays) RB in vitro, whereas ORF13, bearing a point mutation in the RB-binding motif (ORF13*), did not. Increased cell divisions in the vegetative shoot apical meristem and accelerated formation of leaf primordia were observed in plants expressing orf13, whereas the expression of orf13* had no influence on cell division rates in the shoot apical meristem, suggesting a role of RB in the regulation of the cell cycle in meristematic tissues. On the other hand, ectopic expression of LeT6 was not dependent on a functional RB-binding motif. Hormone homeostasis was only altered in explants of leaves, whereas in the root no effects were observed. We suggest that ORF13 confers meristematic competence to cells infected by A. rhizogenes by inducing the expression of KNOX genes and promotes the transition of infected cells from the G1 to the S phase by binding to RB.

Base Sequence↗

PubMed2006

DAWDLE, a forkhead-associated domain gene, regulates multiple aspects of plant development.

Phosphoprotein-binding domains are found in many different proteins and specify protein-protein interactions critical for signal transduction pathways. Forkhead-associated (FHA) domains bind phosphothreonine and control many aspects of cell proliferation in yeast (Saccharomyces cerevisiae) and animal cells. The Arabidopsis (Arabidopsis thaliana) protein kinase-associated protein phosphatase includes a FHA domain that mediates interactions with receptor-like kinases, which in turn regulate a variety of signaling pathways involved in plant growth and pathogen responses. Screens for insertional mutations in other Arabidopsis FHA domain-containing genes identified a mutant with pleiotropic defects. dawdle (ddl) plants are developmentally delayed, produce defective roots, shoots, and flowers, and have reduced seed set. DDL is expressed in the root and shoot meristems and the reduced size of the root apical meristem in ddl plants suggests a role early in organ development.

Alleles↗

PubMed1996

Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase.

The development of clustered tertiary lateral roots (proteoid roots) and the expression of phosphoenolpyruvate carboxylase (PEPC, EC 4.1.1.31) in roots were studied in white lupin (Lupinus albus L.) grown with either 1 mM P (+P-treated) or without P (-P-treated). The +P-treated plants initiated fewer clustered tertiary meristems and the emergence of these meristems was delayed compared with - P-treated plants. Proteoid root zones could be identified 9 d after emergence in both P treatments. Amounts of PEPC mRNA, PEPC specific activity, and enzyme protein were greater in proteoid roots than in normal roots beginning at 10, 12, and 14 d after emergence, respectively. The increases in PEPC mRNA, PEPC enzyme, and PEPC specific activity suggest that this enzyme is in part under transcriptional regulation. Recovery of organic acids from root exudates coincided with the increases in PEPC specific activity. The -P-treated plants exuded 40-, 20-, and 5-fold more citrate, malate, and succinate, respectively, than did +P-treated plants. Data presented support the hypothesis that white lupin has concerted regulation of proteoid root development, transcriptional regulation of PEPC, and biosynthesis of organic acids for exudation in response to P deficiency.

Fabaceae↗

PubMed2000

Can meristematic activity determine variation in leaf size and elongation rate among four Poa species? A kinematic study.

We studied inherent variation in final leaf size among four Poa spp. that live at different elevations. The average final length of leaf 7 of the main stem of the smallest species (Poa alpina) was only one-half that of the largest species (Poa trivialis); it was correlated with leaf elongation rate, but not with the duration of leaf elongation. A faster rate of leaf elongation rate was associated with (a) larger size of the zone of cell expansion, and (b) faster rates of cell production (per cell file) in the meristem, which in turn were due to greater numbers of dividing cells, whereas average cell division rates were very similar for all species (except Poa annua). Also we found that the proliferative fraction equaled 1 throughout the meristem in all species. It was remarkable that rates of cell expansion tended to be somewhat higher in the species with slower growing leaves. We discuss the results by comparing the spatial and material viewpoints, which lead to different interpretations of the role of cell division. Although the presented data do not strictly prove it, they strongly suggest a regulatory role for cell division in determining differences in growth rate among the present four Poa spp.

Biomechanical Phenomena↗

PubMed2002

YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis.

The YABBY (YAB) genes specify abaxial cell fate in lateral organs in Arabidopsis. Loss-of-function mutants in two early-expressing YAB genes, FILAMENTOUS FLOWER (FIL) and YAB3, do not exhibit vegetative phenotypes as a result of redundancy. Mutations in these genes result in the derepression of the KNOX homeobox genes SHOOTMERISTEMLESS (STM), BREVIPEDICELLUS, and KNAT2 in the leaves and in the partial rescue of stm mutants. Here, we show that fil yab3 double mutants exhibit ectopic meristem formation on the adaxial surfaces of cotyledons and leaf blades. We propose that in addition to abaxial specification, lateral organ development requires YAB function to downregulate KNOTTED homeobox genes so that meristem initiation and growth are restricted to the apex.

Alleles↗

PubMed2002

Regulation of axis determinacy by the Arabidopsis PINHEAD gene.

Plants produce proximal-distal growth axes with two types of growth potential: they can be indeterminate, in which case growth continues indefinitely, or they can be determinate, in which case growth is limited to the production of a single organ or a discrete set of organs. The indeterminate shoot axes of Arabidopsis pinhead/zwille mutants frequently are transformed to a determinate state. PINHEAD (PNH) is expressed in the central domain of the developing plant: the provascular tissue, the shoot apical meristem, and the adaxial (upper) sides of lateral organ primordia. Here, we show that ectopic expression of PNH on the abaxial (lower) sides of lateral organs results in upward curling of leaf blades. This phenotype correlates with a loss of cell number coordination between the two surfaces of the blade, indicating that ectopic PNH can cause changes in cell division rates. More strikingly, moving PNH expression from the central to the peripheral domain of the embryo causes transformation of the determinate cotyledon axis to an indeterminate state. We propose that growth axes are specified as determinate versus indeterminate in a PNH-mediated step. Our results add to a growing body of evidence that radial positional information is important in meristem formation. These results also indicate that genes regulating cell division and axis determinacy are likely to be among PNH targets.

Arabidopsis↗

PubMed2006

Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development.

Shoot branching is a major determinant of variation in plant stature. Branches, which form secondary growth axes, originate from stem cells activated in leaf axils. The initial steps by which axillary meristems (AMs) are specified and their stem cells organized are still poorly understood. We identified gain- and loss-of-function alleles at the Arabidopsis thaliana REGULATOR OF AXILLARY MERISTEMS1 (RAX1) locus. RAX1 is encoded by the Myb-like transcription factor MYB37 and is an Arabidopsis homolog of the tomato (Solanum lycopersicum) Blind gene. RAX1 is transiently expressed in a small central domain within the boundary zone separating shoot apical meristem and leaf primordia early in leaf primordium development. RAX1 genetically interacts with CUP-SHAPED COTYLEDON (CUC) genes and is required for the expression of CUC2 in the RAX1 expression domain, suggesting that RAX1 acts through CUC2. We propose that RAX1 functions to positionally specify a stem cell niche for AM formation. RAX1 also affects the timing of developmental phase transitions by negatively regulating gibberellic acid levels in the shoot apex. RAX1 thus defines a novel activity that links the specification of AM formation with the modulation of the rate of progression through developmental phases.

Alleles↗

PubMed2004

High-resolution boundary analysis during Arabidopsis thaliana flower development.

We report a comparative analysis of cell proliferation patterns during Arabidopsis flower development. Cell division was evaluated by a direct method, i.e. the 5-bromo-2'-deoxyuridine (BrdU) incorporation/immunodetection procedure. BrdU patterns in wild-type plants were correlated with the expression profiles of both several cell cycle genes involved in the control of the G(1)/S transition and cell cycle-related repressor genes, MSI4 and MSI5, encoding WD-repeat proteins. To evaluate how proliferation patterns arise with respect to boundaries and vice versa, the expression of a boundary gene, CUP SHAPED COTYLEDON (CUC)2, was determined. Combining these approaches, we demonstrate that boundaries between inflorescence and floral meristems and between floral whorls are narrow bands of non-dividing cells. In addition, we show that negative and positive regulators of cell proliferation are simultaneously and continuously expressed in dividing meristematic domains, being excluded from boundary cells. Finally, BrdU incorporation and CUC2 in situ hybridisation patterns were analysed in two mutant backgrounds, agamous (ag)-1 and superman (sup)-1, in order to assess changes in boundary establishment and different levels of indeterminacy under conditions of altered proliferation at the floral meristem centre.

Arabidopsis↗

PubMed2005

A protocol to analyse cellular dynamics during plant development.

In vivo microscopy generates images that contain complex information on the dynamic behaviour of three-dimensional (3D) objects. As a result, adapted mathematical and computational tools are required to help in their interpretation. Ideally, a complete software chain to study the dynamics of a complex 3D object should include: (i) the acquisition, (ii) the preprocessing and (iii) segmentation of the images, followed by (iv) a reconstruction in time and space and (v) the final quantitative analysis. Here, we have developed such a protocol to study cell dynamics at the shoot apical meristem in Arabidopsis. The protocol uses serial optical sections made with the confocal microscope. It includes specially designed algorithms to automate the identification of cell lineage and to analyse the quantitative behaviour of the meristem surface.

Anatomy, Cross-Sectional↗