Journal of Experimental Botany, Vol. 52, No. 90001, pp. 403-411,
March 2001
© 2001 Oxford University Press
The peri-cell-cycle in Arabidopsis
Vakgroep Moleculaire Genetica en Departement Plantengenetica, Vlaams Interuniversitair Instituut voor Biotechnologie (VIB), Universiteit Gent, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium
Received 23 March 2000; Accepted 10 July 2000
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Abstract |
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The root systems of plants proliferate via de novo formed meristems originating from differentiated pericycle cells. The identity of putative signals responsible for triggering some of the pericycle cells to re-enter the cell cycle remains unknown. Here, the cell cycle regulation in the pericycle of seedling roots of Arabidopsis thaliana (L.) Heynh. is studied shortly after germination using various strategies. Based on the detailed analysis of the promoter-ß-glucuronidase activity of four key cell cycle regulatory genes, combined with cell length measurements, microdensitometry of DNA content, and experiments with a cell cycle-blocking agent, a model is proposed for cell cycle regulation in the pericycle at the onset of lateral root initiation. The results clearly show that before the first lateral root is initiated, the pericycle consists of dissimilar cell files in respect of their cell division history. Depending on the distance behind the root tip and on position in relation to the vascular tissue, particular pericycle cells remain in the G2 phase of the cell cycle and are apparently more susceptible to lateral root initiation than others.
Key words: Cell cycle, lateral root initiation, pericycle, root branching.
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Introduction |
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One of the fundamental questions in developmental biology relates to how cells proliferate and organize themselves to form discrete organs. Unlike animals, in which organogenesis occurs primarily in the embryo, normal growth in plants involves both embryonic and post-embryonic organogenesis. The primary shoot and root apical meristems are formed as a part of the developing embryo and generate the cells that divide to form the shoot and root, respectively. In recent years, the understanding of the basic molecular mechanisms that regulate cell division in plants has progressed considerably. In active meristems, cells are driven through the successive phases of the cell cycle (S, G2, M, and G1) by the formation and activation of different heterodimeric serine/threonine protein kinases (Mironov et al., 1999
). These kinases consist of a catalytic subunit, the cyclin-dependent kinase (CDK), and an activating subunit, a cyclin. CDK activity is regulated at various levels, such as expression, differential subcellular localization, phosphorylation, proteolysis, and interaction with regulatory proteins. Nevertheless, several questions remain to be addressed, especially regarding the developmental and environmental control of cell division. One such question is how cell division is re-initiated in cells that have left the cell cycle. To approach this problem at the molecular level, the choice of an appropriate developmental process is indispensable. A classic example in plants of such a process is the initiation of lateral roots. The root system must proliferate via de novo formed meristems originating from differentiated pericycle cells. Most studies suggest that this happens some distance away from the root apical meristem in the differentiation zone of the root, where pericycle cells are not actively dividing. Consequently, lateral root initiation involves re-entry of cells into the cell cycle. The study of this re-entry process necessitates a good knowledge of the cell cycle behavior of pericycle cells, in particular of those that will give rise to new primordia.
In a previous study, timing and site of the first lateral root initiation event after germination have been determined using Arabidopsis thaliana plants transformed with a promoter-ß-glucuronidase (GUS) fusion for a mitotic cyclin (Arath;CycB1;1) (Dhooge et al., 1999). Initiation of the first lateral root, formed in the acropetal sequence, was found to occur within the first 48 h after germination at a relatively constant distance from the root tip.
Here, the cell cycle regulation of pericycle cells was analysed prior to and during the initiation of a new lateral root primordium. In a first set of experiments, the cell cycle regulation was defined, based on the promoter activity of four cell cycle genes that are expressed at different intervals of the cell cycle. The promoter-GUS fusions for two CDKs (Cdc2aAt and Cdc2bAt) and two cyclins (CycB1;1 and CycA2;1) have previously been proven to be elegant molecular markers for cell cycle studies at the whole plant level (Hemerly et al., 1993; Ferreira et al., 1994; de Almeida Engler et al., 1999). The Cdc2aAt gene is transcribed throughout the cell cycle at a constant level (Martinez et al., 1992; Hemerly et al., 1993) whereas Cdc2bAt is preferentially expressed from the S phase to the G2 (Segers et al., 1996). The CycB1;1 transcript levels rise during the G2 phase, reaching a maximum at the G2-to-M transition, whereas the CycA2;1 expression rises during the S phase, reaches a maximum at the end of G2, and is down-regulated during the early M phase (Shaul et al., 1996).
To get a better insight into the cell cycle behaviour of distinct pericycle cell files, the GUS expression data of the different cell cycle genes were compared with measurements of cell sizes and DNA contents. Furthermore, the effect on lateral root initiation of an arrest of cell cycle progression during S phase was studied on hydroxyurea-containing medium. A model for cell cycle regulation in the pericycle prior to and at the moment of lateral root initiation is proposed.
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Materials and methods |
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Plant material and growth conditions
Seeds from Arabidopsis thaliana (L.) Heynh. (ecotype C24) and transgenic lines expressing the bacterial reporter gene GUS under the control of the Cdc2aAt, Cdc2bAt, Arath;CycA2;1, and Arath;CycB1;1 promoters were sown on a modified agar-solidified Hoagland medium with 0.3% sucrose (Beemster and Baskin, 1998
). After 48 h of stratification at 4 °C, square tissue agar plates (Greiner Labortechnik, Frickenhausen, Germany) were placed vertically in a growth chamber under continuous light (23 °C). For the hydroxyurea treatments, the same growth medium was used with addition of 10 or 100 mM hydroxyurea. For all experiments, except for the hydroxyurea treatments, the seedlings were harvested 40 h after germination.
Microscopy
Histochemical assays of GUS activity were performed and stained whole seedlings were analysed as described previously (Beeckman and Engler, 1994). For detailed anatomical studies, GUS-stained roots were embedded and sectioned in Technovit 7100 (Heraeus Kulzer, Wehrheim, Germany) (Beeckman and Viane, 2000). Sections of 5 µm thickness were stained for 20 min in fresh 0.05% ruthenium red (Fluka Chemie, Buchs, Switzerland), analysed and photographed using an Axioskop microscope (Carl Zeiss, Jena, Germany).
Cell length measurements
Pericycle cells were measured on longitudinal sections (see above) using a graphical tablet SummaSketchTM (Summagraphics, Scottsdale, AZ, USA) and a light microscope M20 (Wild, Heerbrugg, Switzerland) equipped with camera lucida. Serial transverse sections of 5 µm thickness (see above) were made through seedling roots (40 h after germination) from the root tip up to the base of the hypocotyl. For each pericycle cell file, nuclei were counted, starting from the region where the first two sieve elements were differentiated. The distance between the most ‘proximal’ and most ‘distal’ nuclei was determined by multiplying the number of sections between these two points by section thickness (5 µm). Mean cell length in each cell file was then calculated by dividing this distance by the number of nuclei minus 1.
In situ relative DNA content quantification
To quantify relative DNA contents of the discrete pericycle cell files, serial transverse sections through roots of 40-h-old seedlings were made as described above. To increase the probability to hit complete nuclei in one section, the section thickness was 6 µm. Sections were first stained for 20 min in 0.05% ruthenium red, followed by a brief rinse in distilled water, and subsequently stained with 0.1 µg ml–1 4',6-diamidino-2-phenylindole (DAPI) (Katsuhara and Kawasaki, 1996). The prestaining with ruthenium red assured a weak fluorescence of the cell walls, thus allowing a better localization of the discrete pericycle cells.
After staining, sections were mounted in Vectashield (Vector Laboratories, Burlingame, UK). The DAPI was visualized using the filter set 02 on an Axioskop fluorescence microscope (Carl Zeiss) and quantified with a microscope photometer (MPM 100; Zeiss). The measured values were pooled in two groups, namely from nuclei lying at the phloem poles and at the xylem poles. Per group the values were ordered in histograms (see Fig. 4) according to their relative position from the root tip. The DAPI fluorescence in metaphase cells from the same sections was included as reference for a 4C value.
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Results |
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Cell cycle gene expression
In a previous study (Dhooge et al., 1999
), CycB1;1 was found to be expressed in the lateral root founder cells at the advent of the first division. This early GUS expression pattern allowed the determination of the timing and site of the first lateral root initiation event after germination. In brief, the first lateral is initiated in the distal part of the root approximately 1.40±0.28 mm (SE) from the root tip, which happens at the earliest 32 h after germination onwards. In a sample taken 40 h after germination, 29% of the seedlings had one initiation site, 13% more than one, and 58% had none. As a result, this stage provided enough material to study cell cycle regulation in the pericycle prior to and just at the moment of lateral root initiation. Therefore, this stage was chosen to analyse the expression pattern of the four reporter genes, namely Cdc2a-gus, Cdc2b-gus, CycB1;1-gus, and CycA2;1-gus.
Cdc2a-gus was strongly expressed in the root tips (all cell files of the meristem) and in the entire vascular cylinder (pericycle and stelar parenchyma cells) of roots with (Fig. 1A, E) and without initiation sites (data not shown). At this stage, Cdc2b-gus was very faintly expressed in the root tips, in the adventitious root primordia formed at the root–hypocotyl junction, and in the stomata of the cotyledons (Fig. 1B). It was absent from pericycle cells that were not experiencing an initiation event and appeared from the moment lateral roots were initiated, in the lateral root founder cells (Fig. 1F).
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The CycB1;1-gus expression pattern was comparable to that of Cdc2b-gus, being present at the root–hypocotyl junction and the stomata. In the root, it was strongly expressed in the meristem and absent from the entire pericycle, where it appeared only when laterals were initiated (Fig. 1C
, G).
The CycA2;1-gus expression pattern seemed more complicated. It was strongly expressed in the root apical meristems (Figs 1D; 2E, F) and, in contrast to CycB1;1, expression continued for a few 100 µm in the central cylinder above the meristem (Fig. 1D). Serial sectioning showed the GUS precipitate in this zone was present in pericycle cells as well as in stelar parenchyma cells (Fig. 2D). Above this zone, CycA2;1-gus disappeared or became very faint in the vascular cylinder, including the pericycle (Fig. 2C). Higher up in the root, irrespective of the presence of an initiation site, CycA2;1-gus expression re-appeared in the central cylinder (Fig. 2A). Serial sections in this zone showed the staining to be localized in the stelar parenchyma cells, in pericycle cells at the xylem poles and, interestingly, to be absent from the other pericyle cells (Fig. 2B). When initiation occurred, CycA2;1-gus was also strongly expressed during the early stages (Fig. 1H).
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Cell length measurements
The difference in CycA2;1-gus expression pattern between xylem pericycle cells compared to other pericycle cells and the peculiar position in lateral root initiation occupied by these cells, prompted the investigation of possible differences in cell division history between these types of pericycle cells. Therefore, on longitudinal sections, the length of pericycle cells in roots of seedlings where no initiation had taken place was determined (see Materials and methods).
Cell lengths were divided into three groups depending on the position of the pericycle cell files: at the xylem pole, at the phloem pole, and in between. Cells at the phloem poles and the intermediate pericycle cells were similar in length (77.205±2.356 µm and 74.957±3.837 µm), whereas the pericycle cells at the xylem poles were shorter (64.155±4.187 µm) (n=0–50).
As it is difficult to measure enough pericycle cells in intermediate regions on longitudinal sections, another method was used to calculate the pericycle cell length based on the number of nuclei in a series of sections with known thickness (see Materials and methods). Three groups of pericycle cell files were distinguished depending on their location with respect to the vascular tissues. The mean cell length of six roots 40 h after germination is given in Fig. 3. Again, pericycle cells opposite the xylem poles were shorter than the other pericycle cells. Mean cell lengths were also comparable to the values measured on sections.
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DNA measurements
On serial transverse sections from 10 seedling roots at 40 h after germination, the relative DNA contents of the individual pericycle nuclei at the xylem poles and phloem poles were determined (see Materials and methods). The fluorescence of metaphase cells, in sections of the same kind through the root apical meristem, were used as a reference point. Representative histograms are shown for a root without (Fig. 4A, C) and with lateral initiation event in the distal region (Fig. 4B, D). In both root types, G2 values were only found in some cells at the xylem poles and always in the upper half of the root (Fig. 4A, B). In all roots analysed, phloem pericycle cells showed predominantly G1 values (Fig. 4C, D). In roots with early initiation events, groups of G2 cells could clearly be recognized at the site where the first divisions took place.
Hydroxyurea experiments
Hydroxyurea blocks cycling cells during S phase by inhibiting ribonucleotide reductase (Shaul et al., 1996). Hydroxyurea was used to elucidate the point in the cell cycle at which founder cells were arrested. If the founder cells for lateral root initiation were blocked in a G1 phase of the cell cycle, incubation of these roots in hydroxyurea would inhibit the initiation and no CycB1;1-gus expression in the pericycle would be observed. On the other hand, if the founder cells stayed in the G2 phase before being triggered to divide, a G1 block would have no effect on the first round of cell division and CycB1;1-gus expression would point out at least the first round of cell division.
Based upon previous data obtained using the promoter-gus fusion for the CycB1;1 gene, seedlings at 24 h after germination showed no lateral root initiation in the pericycle (Dhooge et al., 1999). Therefore, seedlings at this stage were transferred to 10 and 100 mM hydroxyurea and stained for CycB1;1-gus expression after 48 h and 72 h of incubation. As control, a part of the seedlings was transferred to Hoagland medium (see Materials and methods).
In roots transferred to the control medium, several stages of lateral root formation could be seen (Fig. 5A). The most developed root primordia reached the point of emergence from the parent root (Fig. 5B).
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In roots that had been incubated on hydroxyurea for 48 h and 72 h, several lateral root initiation sites became visible because of the CycB1;1-gus expression. Closer examination of these sites in cleared preparations revealed that the staining was restricted to only a small group of founder cells or to their immediate derivatives. In contrast to the control plants, no more developed lateral root primordia were found.
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Discussion |
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The initiation of the first lateral root primordium after germination was chosen as a model system to study the cell cycle regulation in the pericycle of Arabidopsis. Forty hours after germination, the founder cells in the pericycle switch in approximately 30% of the seedlings from a non-dividing to a dividing state (Dhooge et al., 1999
). In a first set of experiments, the expression patterns of four cell cycle genes was analysed using the gus reporter system. Based on these expression patterns combined with the data from DNA measurements, the model presented in Fig. 6 is proposed.
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In the root tip (Fig. 6
, zone A), all four GUS markers are expressed. Consistently, cell division is active in most of the cell files of the meristem. Although each GUS marker had its own staining pattern in the root tip, no differences between the pericycle cells were found. However, in the mature pericycle, differences in cell length between pericycle cells at the xylem poles and the intervening ones were noted. Such differences in length between mature cells must reflect differences in the number of transverse divisions of the cells from which they arise in the root tip, because sliding of cells occurs rarely in root tissues (Webster and MacLeod, 1980; Casero et al., 1989). Similar differences in pericycle cells were reported in Allium cepa and Pisum sativum (Lloret et al., 1989). As in the case of Arabidopsis, pericycle cells located opposite xylem poles were shorter than cells lying opposite phloem poles. In both species lateral root primordia originated opposite xylem poles. In a species with lateral root initiation occurring at the phloem poles, shorter pericycle cells were found opposite these poles, even in regions of the primary root that is located close to the root tip (Lloret et al., 1989). These observations indicate that differential cell cycle regulation in the pericycle cell files, near or within the root tip, may be crucial for the patterning of root branching. However, not every pericycle cell opposite a given protoxylem (or protophloem) pole is involved in lateral root initiation. Therefore, the observed structural differences are not sufficient to understand root branching. Other control mechanisms on cell cycle regulation must be acting within these pericycle cell files (see also Skene, 2000).
In the provascular cylinder including the pericycle, GUS staining was observed only for Cdc2aAt and CycA2;1 in cells above the root meristem (Fig. 6, zone B), suggesting that these cell files leave the cell cycle at a later time point than the cortical and epidermal cell files. The pericycle cells together with provascular cells move from G1 to G2 via S phase, as implied by the CycA2;1 expression. The cortex and epidermis might stop the cell cycle completely and may enter a G0 phase, or may be the subject of endoreduplication. Further research is needed to clarify their cell cycle behaviour in this zone. The observed cell file-dependent exit from the cell cycle supports earlier views that a root meristem does not have a sharp distal boundary with the elongation zone, but is rather composed of proliferation zones of different length (Barlow, 1984; Casero et al., 1989).
Immediately above this zone (Fig. 6, zone C), CycA2;1 expression diminishes or disappears completely from the pericycle indicating a progression through the cycle via mitosis to a G1 phase. This observation is in agreement with the microdensitometric measurements, which show predominantly a 2C DNA content in all pericycle cells in this zone.
Xylem pericycle cells, however, do not leave the cell cycle completely as is the case for the outer tissue layers. First, the pericycle shows the presence of Cdc2aAt-gus expression throughout the whole root, indicating the maintenance of cell division competence. Secondly, CycA2;1-gus expression diminishes only in a narrow zone above the root meristem, but reappears in xylem pericycle cells in the upper half of the seedling root (Fig. 6, zone D). Likewise, in sections of Raphanus sativus roots that were hybridized with a radioactively labelled CycA2;1 mRNA fragment, strong labelling was observed preferentially in pericycle cells at the xylem poles (Burssens et al., 2000).
Furthermore, two lines of evidence suggest that those pericycle cells that will give rise to a lateral root remain in the G2 phase of the cycle. Firstly, when seedling roots, at a stage before laterals could be initiated, were treated with hydroxyurea, the very first divisions in the founder cells could still take place, while further development was blocked immediately thereafter by the inhibition of the S phase transition. Secondly, the few 4C values were all recorded in that part of the root where the initiation of the first lateral is to be expected.
Although phloem pericycle cells also show Cdc2aAt-gus expression throughout the whole root, no CycA2;1 expression could be observed in the distal root part. Taking into account their 2C DNA content, these cells most probably remain in the G1 phase of the cell cycle.
These data together with the cell length measurements allow the conclusion to be drawn that, at least in Arabidopsis, the pericycle is composed of dissimilar cell files. The cells adjacent to the phloem poles reach their maturation after fewer cell divisions and remain in the G1 phase whereas the xylem pericycle cells undergo more divisions in the meristem itself, do not remain in the G1 phase, but proceed to the G2 phase in the upper half of the seedling root where they may receive a signal to divide and start the initiation of a new primordium. The reason why xylem pericycle cells seem to be more susceptible to lateral root initiation in most plants may result from the fact that these cells have completed DNA synthesis and remain at the phase that immediately precedes the M phase. This hypothesis fits nicely with the ‘primed pericycle model’ of Skene (Skene, 2000). In this model, pericycle cells at the protoxylem poles become primed by a radial factor. Only a subset of these primed (G2) cells will be triggered later on by a longitudinally distributed factor. It has been well documented that auxin has a promotive effect on lateral root initiation (Blakely et al., 1982; Boerjan et al., 1995; Celenza et al., 1995; Laskowski et al., 1995). Therefore, this plant hormone could play a dominant role in both priming and triggering the pericycle cells. However, the precise link on the molecular level between auxin and cell division has still to be clarified. Finally, the presence of both types of pericycle cells also explains the conflicting ideas found in literature in which pericycle cells were first thought to be arrested in G1 (Corsi and Avanzi, 1970) and later in G2 (Blakely and Evans, 1979).
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Acknowledgments |
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The authors thank Sandra Dhooge, Ive De Smet, and Roeland Nieuwborg for help with microdensitometric measurements, Dr Keith Skene (Department of Biological Sciences, University of Dundee, UK) for helpful comments, Martine De Cock for help in preparing the manuscript, and Stijn Debruyne for figures.
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Notes |
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1 To whom correspondence should be addressed. Fax : +32 9 264 5349. E-mail: diinz{at}gengenp.rug.ac.be
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References |
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S. Vanneste, B. De Rybel, G. T.S. Beemster, K. Ljung, I. De Smet, G. Van Isterdael, M. Naudts, R. Iida, W. Gruissem, M. Tasaka, et al. Cell Cycle Progression in the Pericycle Is Not Sufficient for SOLITARY ROOT/IAA14-Mediated Lateral Root Initiation in Arabidopsis thaliana PLANT CELL, November 1, 2005; 17(11): 3035 - 3050. [Abstract] [Full Text] [PDF]
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 L. Laplaze, B. Parizot, A. Baker, L. Ricaud, A. Martiniere, F. Auguy, C. Franche, L. Nussaume, D. Bogusz, and J. Haseloff GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana J. Exp. Bot., September 1, 2005; 56(419): 2433 - 2442. [Abstract] [Full Text] [PDF]
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T. Pasternak, G. Potters, R. Caubergs, and M. A. K. Jansen Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level J. Exp. Bot., August 1, 2005; 56(418): 1991 - 2001. [Abstract] [Full Text] [PDF]
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C. Sorin, J. D. Bussell, I. Camus, K. Ljung, M. Kowalczyk, G. Geiss, H. McKhann, C. Garcion, H. Vaucheret, G. Sandberg, et al. Auxin and Light Control of Adventitious Rooting in Arabidopsis Require ARGONAUTE1 PLANT CELL, May 1, 2005; 17(5): 1343 - 1359. [Abstract] [Full Text] [PDF]
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K. Ljung, A. K. Hull, J. Celenza, M. Yamada, M. Estelle, J. Normanly, and G. Sandberg Sites and Regulation of Auxin Biosynthesis in Arabidopsis Roots PLANT CELL, April 1, 2005; 17(4): 1090 - 1104. [Abstract] [Full Text] [PDF]
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K. Zhang, L. Diederich, and P. C.L. John The Cytokinin Requirement for Cell Division in Cultured Nicotiana plumbaginifolia Cells Can Be Satisfied by Yeast Cdc25 Protein Tyrosine Phosphatase. Implications for Mechanisms of Cytokinin Response and Plant Development Plant Physiology, January 1, 2005; 137(1): 308 - 316. [Abstract] [Full Text] [PDF]
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 K. Himanen, M. Vuylsteke, S. Vanneste, S. Vercruysse, E. Boucheron, P. Alard, D. Chriqui, M. Van Montagu, D. Inze, and T. Beeckman Transcript profiling of early lateral root initiation PNAS, April 6, 2004; 101(14): 5146 - 5151. [Abstract] [Full Text] [PDF]
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G. Hou, J. P. Hill, and E. B. Blancaflor Developmental anatomy and auxin response of lateral root formation in Ceratopteris richardii J. Exp. Bot., March 1, 2004; 55(397): 685 - 693. [Abstract] [Full Text] [PDF]
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M. Konishi and M. Sugiyama Genetic analysis of adventitious root formation with a novel series of temperature-sensitive mutants of Arabidopsis thaliana Development, December 1, 2003; 130(23): 5637 - 5647. [Abstract] [Full Text] [PDF]
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K. Himanen, C. Reuzeau, T. Beeckman, S. Melzer, O. Grandjean, L. Corben, and D. Inze The Arabidopsis Locus RCB Mediates Upstream Regulation of Mitotic Gene Expression Plant Physiology, December 1, 2003; 133(4): 1862 - 1872. [Abstract] [Full Text]
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H. Ullah, J.-G. Chen, B. Temple, D. C. Boyes, J. M. Alonso, K. R. Davis, J. R. Ecker, and A. M. Jones The {beta}-Subunit of the Arabidopsis G Protein Negatively Regulates Auxin-Induced Cell Division and Affects Multiple Developmental Processes PLANT CELL, February 1, 2003; 15(2): 393 - 409. [Abstract] [Full Text] [PDF]
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K. Himanen, E. Boucheron, S. Vanneste, J. de Almeida Engler, D. Inze, and T. Beeckman Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation PLANT CELL, October 1, 2002; 14(10): 2339 - 2351. [Abstract] [Full Text] [PDF]
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J. E. Malamy and K. S. Ryan Environmental Regulation of Lateral Root Initiation in Arabidopsis Plant Physiology, November 1, 2001; 127(3): 899 - 909. [Abstract] [Full Text] [PDF]
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A. Marchant, R. Bhalerao, I. Casimiro, J. Eklof, P. J. Casero, M. Bennett, and G. Sandberg AUX1 Promotes Lateral Root Formation by Facilitating Indole-3-Acetic Acid Distribution between Sink and Source Tissues in the Arabidopsis Seedling PLANT CELL, March 1, 2002; 14(3): 589 - 597. [Abstract] [Full Text] [PDF]
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