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Plant Physiology 133:1862-1872 (2003) © 2003 American Society of Plant Biologists The Arabidopsis Locus RCB Mediates Upstream Regulation of Mitotic Gene Expression1Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology, Ghent University, Technologiepark 927, B-9052 Gent, Belgium (K.H., T.B., L.C., D.I.); CropDesign N.V., B-9052 Gent, Belgium (C.R.); Université de Liège, Sart-Tilman, B-4000 Liège, Belgium (S.M.); and Institut National de la Recherche Agronomique, Centre de Versailles, Route de Saint-Cyr, F-78026, France (O.G.)
Transcriptional regulation of cell cycle regulatory genes, such as B-type cyclins, is tightly linked with the mitotic activity in the meristems. To study the regulation of a B-type cyclin gene, a targeted genetic approach was undertaken. An Arabidopsis line containing a fusion construct between the CYCB1;1 promoter and a bacterial  -glucuronidase marker gene (uidA) was used in ethyl methanesulfonate mutagenesis. The mutants were screened for altered CYCB1;1::uidA expression patterns. In a reduced CYCB1;1 expression mutant (rcb), the CYCB1;1::uidA expression was severely affected, being excluded from the shoot and root apical meristems and leaf primordia and shifted to cells associated with root cap and stomata. In addition to the overall reduction of the endogenous CYCB1;1 transcript levels, other G2-to-M phase-specific genes were also down-regulated by the mutation. In the mutant plants, the inflorescence stem growth was reduced, indicating low meristem activity. Based on the altered CYCB1;1::uidA expression patterns in rcb root meristem, a model is proposed for RCB that mediates the tissue specificity of CYCB1;1 promoter activity.
The eukaryotic cell cycle is controlled at two major checkpoints, one before DNA replication (G1 to S) and one before mitosis (G2 to M). In yeast (Saccharomyces cerevisiae) and animals, progression through these checkpoints is driven by cyclin-dependent kinases (CDKs), the activity of which depends on interaction with their regulatory subunits, the cyclins. Different cyclins mediate the cell cycle phase-specific activation of the CDKs and modify their substrate specificity in a spatial and temporal manner (Stals and Inzé, 2001  ). In Arabidopsis, five classes of CDKs have been identified (Vandepoele et al., 2002), but only two of them have been extensively characterized: CDKA;1 (formerly known as Cdc2a), which is active at the G1-to-S and G2-to-M checkpoints, and CDKB1;1 (formerly known as Cdc2b), whose activity is highest at the G2-to-M-transition (Mironov et al., 1999; Joubès et al., 2000; Porceddu et al., 2001; Menges and Murray, 2002). CDKB1;1 represents a plant-specific CDK that is thought to interact with the mitotic cyclin CYCB1;1 at the G2-to-M transition (Criqui et al., 2000) and also both genes show a coordinated transcriptional up-regulation during the G2-to-M phase (Mironov et al., 1999). Three main classes of cyclins (A, B, and D type) have been described in plants, and in the Arabidopsis genome, a total of 30 cyclins have been identified (Vandepoele et al., 2002). D-type cyclins are preferentially induced by mitogen stimuli at the G1 phase (Soni et al., 1995; Fuerst et al., 1996; Richard et al., 2002). Unlike the D-type cyclins, the levels of A- and B-type cyclins are tightly controlled by cell cycle progression. The promoter activities and transcript levels of A-type cyclins have been shown to increase at mid S phase (Fuerst et al., 1996; Shaul et al., 1996). For B-type cyclins, G2 and M phase-specific peaks in expression have been shown in many plant species, such as Arabidopsis (Ferreira et al., 1994a), Catharanthus roseus (Ito et al., 1998), and Nicotiana sylvestris (Tréhin et al., 1999).
As regulatory proteins, cyclins have a high turnover rate, and their cyclic appearance results from stringent regulation at the transcriptional level (Shaul et al., 1996 Despite extensive analysis of the transcriptional control of the mitotic cyclin CYCB1;1, little is known about the regulatory pathways that affect its promoter activity. In an attempt to study the upstream regulation of the CYCB1;1 promoter, a targeted genetic approach was undertaken. The CYCB1;1::uidA line was used in chemical mutagenesis, thereby allowing visualization of mutations that specifically affect the promoter activity. Mutants were screened for altered patterns of CYCB1;1::uidA expression. We report the identification and characterization of a mutant line with reduced CYCB1;1::uidA expression (designated rcb). The rcb mutant lost CYCB1;1::uidA expression in both shoot and root apical meristems and leaf primordia, whereas the expression was ectopically induced in cells associated with root cap and stomata. In addition, the overall endogenous levels of the CYCB1;1 transcripts and those of other mitotic genes were reduced in the rcb mutant. In mature plants, the total length of the inflorescence stem and its diameter were significantly affected, indicating an effect on the meristem activity. Based on the altered CYCB1;1::uidA expression patterns in rcb root meristems, we propose a model in which RCB mediates the tissue specificity of the CYCB1;1 promoter activity.
Isolation of the rcb Mutant and Genetic Analysis
To study the regulation of the CYCB1;1 promoter activity, 2,000 seeds of the transgenic Arabidopsis line containing a CYCB1;1::uidA promoter fusion (Ferreira et al., 1994b
Before further phenotypic analysis, the mutant line was subjected to three successive backcrosses with the CYCB1;1::uidA starter line. In the F1 population, gain of CYCB1;1::uidA expression in the root cap was detected in all of the progeny, indicating that thercb mutation was semidominant. In the F2 population, three classes of expression patterns were observed. When compared with the homozygous wild-type (RCB/RCB; Fig. 1A) and homozygous mutant plants (rcb/rcb; Fig. 1B), the heterozygous mutants (rcb/RCB; Fig. 1C) had intermediate expression patterns. As with the homozygous mutants, the heterozygous mutants (F1, 100%; and F2, 50%) showed a gain of CYCB1;1::uidA expression in the lateral root cap. In the root apical meristem, however, intermediate intensities of the CYCB1;1::uidA expression were observed, whereas in the homozygous mutants, no expression was detected in that tissue. In the F2 population, the segregation pattern of ectopic CYCB1;1::uidA expression in the root cap again suggested the semidominant nature of the rcb mutation. To further confirm that the rcb mutation was independent from the CYCB1;1::uidA transgene, test crosses were performed between the rcb mutants and the C24 wild-type plants. The CYCB1;1::uidA expression pattern in the F1 population resembled that obtained from the backcrosses, although the GUS staining was often much weaker because of the reduced amount of CYCB1;1::uidA T-DNA in the progeny. In the F2 population, CYCB1;1::uidA-driven GUS staining patterns typical for wild-type (RCB/RCB, 24%), heterozygous (rcb/RCB, 47%), rcb mutant (rcb/rcb, 24%), and GUS-negative (5%) genotypes were encountered. This result confirmed that the mutation was independent from the uidA promoter fusion itself because the wild-type (RCB/RCB) CYCB1;1::uidA expression patterns could be recovered without introducing wild-type alleles of the uidA construct. However, the segregation pattern of the GUS-negative plants was only 5% in the F2 population, indicating that rcb contained two alleles of the uidA transgene. The segregation pattern of GUS-negative lines (5%) was also confirmed by kanamycin selection: Only 10 of 200 F2 plants were sensitive to the selection. This result again underlines the fact that the rcb mutation resides outside the CYCB1;1::uidA fusion because the mutation was able to relocalize the expression of the two CYCB1;1::uidA transgenes.
To determine the genomic locus of the rcb mutation, genetic mapping was initiated with amplified fragment length polymorphism (AFLP) markers (Peters et al., 2001
The rcb mutant was selected on the basis of a remarkable change in the CYCB1;1 promoter-driven GUS staining patterns. To further characterize the cell specificity of the CYCB1;1::uidA expression in rcb roots, the wild-type expression pattern was analyzed in anatomical sections. In the primary root apical meristem of the wild-type plant, the CYCB1;1::uidA expression was detected in a cell type-specific manner in the epidermal and cortical cell files (Fig. 1D), whereas in the newly developed meristems of lateral root primordia, the expression was uniform (Ferreira et al., 1994b
Wild-type shoot apical meristem and emerging leaf primordia expressed CYCB1;1::uidA strongly (Fig. 1F). In young wild-type leaf primordia, the basipetal gradient of cell division activity could be observed (Fig. 1G; see also Donnelly et al., 1999 Also, in rcb flowers, an altered CYCB1;1::uidA expression was observed. In the flowers of wild-type plants, CYCB1;1::uidA expression was strong in developing pistil, excluding the stigma and nectaries (Fig. 1, L and M). In contrast, in the rcb mutant line, no GUS staining was detected in the pistil, whereas the nectaries were strongly stained (Fig. 1, N and O). Thus, in different tissues and organs of the rcb mutant, a shift in CYCB1;1::uidA localization takes place in comparison with the wild type. Both in the root and shoot apical meristems, the strong meristematic CYCB1;1::uidA expression was lost in rcb, whereas an ectopic expression was induced in tissues that usually have no mitotic activity. In addition, the semidominant nature of the rcb mutant indicates that RCB could encode a dose-dependent activator of the CYCB1;1 promoter in meristematic tissues and perhaps a repressor outside the meristems.
In the rcb roots, the CYCB1;1::uidA expression was affected in a cell type-specific manner, namely ectopically induced in the lateral root cap initial cells. We analyzed the CYCB1;1::uidA expression in more detail in wild-type and rcb roots at different stages of root cap development: In rcb, it characteristically changed during root cap development, whereas in wild-type plants, it was high in the developing lateral root primordia (Fig. 2A) until starch accumulated in the newly forming root cap cells (Fig. 2B). Upon differentiation of statocyte layers in the columella, the CYCB1;1::uidA expression diminished (Fig. 2C), and in mature wild-type root caps, it was undetectable (Fig. 2D). In contrast, in rcb, the CYCB1;1::uidA expression followed an opposite pattern and appeared to be tightly linked with the development of the statocyte tissues. In young lateral root primordia (before development of the statocytes), CYCB1;1::uidA was not expressed (Fig. 2, E and F). The CYCB1;1::uidA expression in lateral root caps of rcb appeared with the maturation of the statocytes in the columella (Fig. 2G). At the time the statocyte layers in the columella were fully developed, the lateral root cap cells showed strong GUS staining, whereas the columella remained unstained (Fig. 2H).
In rcb mutants, the CYCB1;1::uidA expression was absent from the root apical meristem and was exclusively associated with the root cap-specified zone. We tested two conditions under which the size and cell patterning of root meristems were severely altered. Treatment with the auxin transport inhibitor naphthylphthalamic acid is known to cause spanning of tissue with root cap identity upwards from the root tip (Sabatini et al., 1999
To analyze the shoot-specific growth phenotypes of rcb, the mutant and CYCB1;1::uidA wild-type plants (C24 ecotype) and the CYCB1;1 knockout line from the Versailles T-DNA collection and the corresponding wild-type plants (Wassilewskija [Ws] ecotype) were grown under short- (8 h/16 h) and long- (16 h/8 h) day light conditions. Growth was analyzed by comparing the number and size of rosette leaves, number of rosette and lateral branches, plant height, flowering time, and flower development. Observations were made on 40 plants in at least three replicates for the growth conditions. Although under constant light conditions no consistent growth phenotypes were detected, under short- and long-day conditions, the growth of rcb plants was considerably altered when compared with that of the wild-type controls (Table I). The growth of rcb plants was repressed at the stage of inflorescence stem development, which were approximately 25% shorter in height and more rigid than the wild-type plants (Fig. 3A). Flowering time in rcb was delayed by approximately 6 d. Rosette leaf growth was similar to that of wild-type controls, without any significant difference in leaf development and leaf number. Rosette branch development was reduced, whereas lateral branches developed as those of control plants. The growth of the CYCB1;1 knockout plants was comparable with that of the wild-type plants, with only a significantly reduced number of leaves and rosette branches in the mutant plants (Table I).
In rcb, the silique length and diameter were significantly shorter (40%) and larger than those of wild-type plants, respectively (Table I). Furthermore, under both long- and short-day conditions, the stem diameter increased significantly in rcb plants from the basis of the rosette when the flowering stem was 2 d old (1-cm total height) until the end of the development. An increase in diameter of the lateral branches of rcb was similarly observed. To identify the origin of the stem diameter increase, the stems were sectioned at different positions, starting from 1 cm above the rosette (below any lateral branches) and at approximately 10 cm from the rosette. The rcb stem sections were larger but had a normal radial symmetry consisting of an epidermal layer, four to five layers of chlorenchyme, a layer of alternating vascular bundles and intervascular fibers, and a central zone. In control plants, the average number of vascular strands in the stem sections was nine, instead of an average of 11 in rcb plants (Fig. 3, B and C). The structure of the vascular strands in rcb differed from that of control plants by larger vascular bundles at the base of the stem and at one-third of the overall stem height. The difference in shape of the vascular bundles appears to be due to an increase in cell size both in the phloem and in the xylem regions (Fig. 3, D and E). Also, the cells between the vascular bundles were enlarged, contributing to the overall expansion of the stem diameter (Fig. 3, F and G). The number of cells in the inflorescence stem was estimated by calculating the number of cells from 10 images taken of sections cut 1 cm above the rosette. Although the cell numbers did not change in the cortex, in the central stele, and especially in the interfascicular zone, considerably more cells were present in rcb than in the wild type (Table I). Kinematic analysis of root growth from germination until 2 weeks of age, quantification of the number of lateral roots, and flow cytometric analysis of root and leaf tissues did not reveal any differences between rcb and wild-type plants (data not shown).
To test whether the rcb mutation affected other cell cycle genes, transcript levels of CYCA2;1, CYCB1;1, CYCB2;1, CDKA;1, and CDKB1;1 were analyzed by semiquantitative RT-PCR as described previously by Himanen et al. (2002
rcb Shows an "Inverse" Development of the CYCB1;1::uidA Expression Pattern during Root Cap Maturation Compared with the Wild Type
The most striking phenotype of the rcb mutant was the ectopic expression of CYCB1;1::uidA observed in the root cap where wild-type plants do not show any expression. Our results indicate that the CYCB1;1::uidA expression pattern is strictly localized in specific cell types, depending on the developmental stage of the particular organ. In the wild-type root apical meristem, the CYCB1;1::uidA is expressed in the dividing cortical and epidermal cell files, whereas in the rcb, no expression is detected. However, during the lateral root development in rcb, the CYCB1;1::uidA expression is only induced upon root cap maturation and becomes restricted to the lateral root cap cells, whereas it is not expressed in the mature root cap of the wild type. In pea (Pisum sativum), the root cap meristem is regulated independently from the primary root apical meristem and is programmed to produce a species-specific amount of root cap cells (Hawes et al., 1998
In Arabidopsis, the border cells appear to be tightly associated with the root cap and are not released during water agitation treatment (Hawes et al., 1998
Based on the phenotypic analysis of the rcb mutant, we conclude that in addition to the regulation of CYCB1;1 tissue specificity in roots, RCB is necessary for inflorescence meristem activity. Plant development is generally due to a balance between cell division in meristematic tissues to produce organs and cell growth and differentiation to allow organ growth and maturation. The stem phenotype appeared rather late, during rosette and inflorescence growth, namely at the onset of inflorescence stem growth. Because the number of lateral organs remained unaltered, the size and the early functioning of the shoot apical meristem were probably not strongly affected. However, the meristem function may be modified at a later stage, perhaps by affecting the cell production rate in the meristem responsible for inflorescence stem growth. Furthermore, increased number of cells in the transverse sections of the inflorescence stems was detected, suggesting that these growth activities are regulated independently from each other.
In the flower organs of wild-type plants, CYCB1;1::uidA expression was found in the young tip of the pistil where actively dividing cells are present (Liu et al., 1997
The rcb mutation affected various organs. In roots and leaves, where changes in CYCB1;1::uidA expression were detected, no growth phenotypes were observed. On the other hand, the inflorescence stem had a strong growth phenotype probably because of the effect of the rcb mutation on the expression of CYCB1;1 in the shoot apex. In addition, a similar response was observed in the siliques, which remained shorter but broader than in wild type. Interestingly, the phenotype of a CYCB1;1 knockout mutant differed from that observed in rcb, showing a decrease in number of rosette leaves and rosette branches. These observations indicate that the tissue specificity of CYCB1;1 expression and CYCB1;1 knockout had a different effect on the shoot apical meristem activity.
In addition to the down-regulation of CYCB1;1, the rcb mutation also down-regulated the M phase-specific genes (CYCB2;1, and CDKB1;1) at the transcriptional level. The fact that the rcb mutant was still able to grow indicated that the functions of these genes have probably been taken over by other genes. These data suggest a high level of redundancy for cell cycle genes in plants. Similar situations are found in yeast with three G1 cyclins (Cln1, Cln2, and Cln3). Only loss-of-function of the Cln3 delays slightly entry into S phase; however, cells that are double mutants for certain combinations of these genes have a more severe cell cycle delay than the single mutants (Thomas, 1993
In mammals, such flexibility does not seem to exist. In mice (Mus musculus), deletion of one of the two B-type cyclins (CycB1) is lethal, although the function of the other, CycB2, can be compensated (Brandeis et al., 1998
Not much is known about the redundancy between plant cyclins. Immunolocalization studies in maize (Zea mays) have revealed different subcellular localizations for several closely related plant cyclins (Mews et al., 1997
We aimed at identifying direct regulators of CYCB1;1 promoter activities. In the rcb mutant, identified from the screen of ethyl methanesulfonate-mutagenized CYCB1;1::uidA plants, a shift in tissue specificity of GUS activity was encountered, indicating that RCB itself may be situated upstream of the CYCB1;1 promoter regulation. Based on the CYCB1;1::uidA expression patterns in wild-type and rcb mutants, we propose a model for the function of RCB. In this model, RCB plays a dual role both as a positive regulator for CYCB1;1 promoter activation in the outer layers of the root apical meristem and as a repressor in lateral root cap cells (Fig. 5A). This conclusion derives from the observed loss of CYCB1;1::uidA expression in the root apical meristem and, on the other hand, on the gain-of-expression in the lateral root cap in rcb (Fig. 5B). Further support for the model comes from the analysis of the heterozygous mutants in which the meristematic expression has been reduced to an intermediate level in combination with a gain-of-expression in the root cap (Fig. 5C). It is interesting that a similar change in CYCB1;1::uidA expression patterns has been observed in the shoot of rcb. The typically strong expression pattern of wild-type plants in the shoot apical meristem is absent in rcb; instead, a shift to parenchyma cells beneath the developing stomata is observed. It is tempting to speculate that RCB encodes a trans-acting factor that would act both as an activator and a repressor, depending on the interaction with other proteins. The existence of trans-acting factors, which act both positively and negatively on the expression of cell cycle genes, is not unprecedented. In animals, the heterotrimeric transcription factor NFY has been shown to transcriptionally inhibit CycB1, CycB2, and Cdc25 promoters upon DNA damage-induced G2 arrest (Manni et al., 2001
Plant Material
The transgenic Arabidopsis line CYCB1;1::uidA (Ferreira et al., 1994b
The Arabidopsis CYCB1;1::uidA promoter fusion line was chemically mutagenized with ethyl methanesulfonate. Treatment with 0.3% (w/v) ethyl methanesulfonate was performed for 12 h, after which the seeds were extensively washed with water. M1 plants were germinated on K1 medium and transferred to soil after 2 weeks of growth for self-fertilization. M2 progenies were analyzed in a GUS assay-based mutant screening. From each line, 25 seeds were germinated together with wild-type controls. Root cuttings were collected for the GUS assay after 1 week of growth. The lines were screened for alterations in the pattern or intensity of the CYCB1;1::uidA expression. The selected putative mutant lines were self-fertilized, and the M3 plants were subjected to three successive backcrosses with the starter line before phenotypic analysis. Intactness of the CYCB1;1::uidA promoter fusion in the mutants was controlled by sequencing. The promoters from both wild type and rcb were isolated by standard PCR amplification with Pfu (Promega, Madison, WI). Primers were designed to hybridize with the flanking sequences on each side of the actual CYCB1;1 promoter in the CYCB1;1::uidA construct and inside the promoter (5'CGCGATCCAGACTGAATGCCCACAGGCCG with 5'CGTGCCACGCGCTACAGACCACGCCC and 5'GGGCGTGGTCTGTAGCGCGTGGCACG with 5'GCCTGGGGTGCCTAATGAGTGAGAATTGACGG). PCR products were run on 0.9% (w/v) agarose gels, purified with Qiaquick Gel Extraction Kit (Qiagen, Hilden, Germany), and sequenced. Sequences from three replicate samples were compared with the promoter from the mutant starter line in multiple alignments (GCG Wisconsin Package; Accelrys, San Diego, CA).
For mapping of the rcb mutant, an AFLP mapping system was used (Vos et al., 1995
For in situ hybridization, the plant material was grown according to the method of Corbesier et al. (1996
For histochemical GUS assays, complete seedlings or root cuttings were stained in multiwell plates (Falcon, Becton-Dickinson, Bedford, MA). GUS assays were performed as described by Beeckman and Engler (1994
For anatomical sections, samples from the GUS assays were fixed overnight in 1% (v/v) glutaraldehyde and 4% (w/v) paraformaldehyde in 50 mM phosphate buffer. Samples were dehydrated and embedded in Technovit 7100 resin (Heraeus Kulzer, Wehrheim, Germany) according to the manufacturer's instructions. For proper orientation of the samples, transparent strips were used to facilitate alignment of the tissues (Beeckman and Viane, 2000
Plants were grown at 20°C in small pots on soil in the greenhouse under long-day conditions (16 h of light/8 h of darkness) with sodium lamps and at 15°C under short-day conditions (8 h of light/16 h of darkness) conditions with cool-white lights (75-100 µE m-2, Philips, Eindhoven, The Netherlands). Stem samples taken at 1 and 10 cm above the rosette were sectioned manually. Tissues samples were treated 20 min in 50% (v/v) sodium hypochlorite, washed in water for 30 min, fixed for 5 min in acetic acid, stained for 5 min in 0.1% (w/v) toluidine blue, and washed in tap water. Samples were examined through a Wild M3 Microscope (Leica) and photographed under bright field. Data were collected and analyzed with Optimas 6.0 (MediaCybernetics, http://www.optimas.com/optimas.htm).
Endogenous transcript levels of a set of cell cycle regulatory genes were analyzed by semiquantitative RT-PCR as described by Burssens et al. (2000b ) and Himanen et al. (2002). For the cDNA synthesis, total RNA was prepared with RNeasy reagents (Qiagen) from 1-week-old wild-type and rcb seedlings. The cDNA was prepared from three independent RNA samples, and 15, 20, and 25 cycles of PCR were tested to verify the exponential phase of the amplification.
The authors acknowledge Christiane Genetello for the effort in maintaining the mutant lines during the project, Janny Peters and Tom Gerats for help in determining the map position of the RCB locus, Katia Belcram for her technical contribution in the identification and analysis of shoot phenotypes, Nathalie Detry for in situ hybridizations, Rebecca Verbanck for artwork, Jan Zethof for INDEL primers, Meeta Mistry for critical reading of the manuscript, and Martine De Cock for help in preparing it. Received May 21, 2003; returned for revision June 25, 2003; accepted September 9, 2003.
1 This work was supported by the Interuniversity Poles of Attraction Program (Belgian State, Prime Minister's Office, Federal Office for Scientific, Technical, and Cultural Affairs, grant no. P5/13), by the Academy of Finland (fellowship to K.H.), and by the Finnish Cultural Foundation for fellowships (fellowship to K.H.). 
2 Present address: Laboratory of Plant Molecular Biology, Rockefeller University, 1230 York Avenue, New York, NY 10021.
3 Present address: University of East Anglia, Norwich NR4 7TJ, UK. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.027128. * Corresponding author; e-mail dirk.inze{at}psb.ugent.be; fax 32-9-3313809.
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