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First published online January 11, 2006; 10.1104/pp.105.074724 Plant Physiology 140:591-602 (2006) © 2006 American Society of Plant Biologists
A Novel Plant-Specific Family Gene, ROOT PRIMORDIUM DEFECTIVE 1, Is Required for the Maintenance of Active Cell Proliferation1Botanical Gardens, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 112–0001, Japan
Hypocotyl segments of Arabidopsis (Arabidopsis thaliana) produce adventitious roots in response to exogenously supplied auxin. root primordium defective 1 (rpd1) is a temperature-sensitive mutant isolated on the basis of impairment in this phenomenon. This study describes further phenotypic analysis of the rpd1 mutant and isolation of the RPD1 gene. When adventitious root formation was induced from the rpd1 explants at the restrictive temperature, cell proliferation leading to root promordia formation was initiated at the same time as in wild-type explants. However, development of the root primordia was arrested thereafter in the mutant. Temperature-shift experiments indicated that RPD1 exerts its function before any visible sign of root primordium formation. The expression patterns of the auxin-responsive gene DR5:  -glucuronidase and the cytodifferentiation marker gene SCARECROW suggest that the rpd1 mutation interferes with neither axis formation nor cellular patterning at the initial stage of root primordium development. Taken together with the effect of the rpd1 mutation on callus cell proliferation, these data imply a role for RPD1 in prearranging the maintenance of the active cell proliferation during root primordium development. Positional cloning of the RPD1 gene revealed that it encodes a member of a novel protein family specific to the plant kingdom. Disruption of the RPD1 gene by a T-DNA insertion caused embryogenesis arrest at the globular to transition stages. This phenotype is consistent with the hypothesized function of RPD1 in the maintenance of active cell proliferation.
The formation of adventitious and lateral roots is a typical example of de novo postembryonic organogenesis that is achieved through the elaborate regulation of cell proliferation. The process of morphogenesis common to adventitious and lateral roots can be summarized as follows. First, cell proliferation is initiated from quiescent cells in response to endogenous or external stimuli, including auxin (Boerjan et al., 1995  ; Celenza et al., 1995; Hobbie and Estelle, 1995; Reed et al., 1998; Tian and Reed, 1999; Xie et al., 2000; Malamy and Ryan, 2001; Nakazawa et al., 2001; Rogg et al., 2001; Fukaki et al., 2002). A rapid increase in cell number leads to the formation of the root primordium (MacLeod and Thompson, 1979; Laskowski et al., 1995). During the development of the root primordium, cellular patterning generates the structure of the root apical meristem (Malamy and Benfey, 1997). Cell proliferation then diminishes and the primordium emerges from the parental tissue mainly by cell elongation (Friedberg and Davidson, 1971; MacLeod and McLachlan, 1975; Malamy and Benfey, 1997). The reactivation of cell proliferation in the root apical meristem after root emergence is dependent on environmental conditions, and in some cases, arrest is maintained for a long time (Celenza et al., 1995; Zhang et al., 1999; Zhang and Forde, 2000; Signora et al., 2001; De Smet et al., 2003). Once the root apical meristem is activated, it becomes responsible for the subsequent growth of the root. Therefore, the regulation of cell proliferation is the central concern of postembryonic root formation.
Previously, we isolated temperature-sensitive mutants of Arabidopsis (Arabidopsis thaliana) that are defective in adventitious root formation (Konishi and Sugiyama, 2003 In this article, we report a detailed phenotypic analysis of the rpd1 mutant and the cloning of the RPD1 gene. We also describe the knockout phenotype of RPD1. Our work implicates the involvement of RPD1 in the maintenance of active cell proliferation and sheds light on the novel plant-specific protein family to which RPD1 belongs.
Effects of rpd1 Mutation on Adventitious Root Formation
When hypocotyl explants of wild-type Arabidopsis are cultured on root-inducing medium (RIM), they generate adventitious roots within several days. Two allelic mutants of the RPD1 locus, rpd1-1 and rpd1-2, were isolated as temperature sensitive for this process (Konishi and Sugiyama, 2003 Closer observation of the time course of adventitious root development showed that the effect of the rpd1 mutation occurred in a stage-specific manner (Fig. 1). When cultured at 28°C, stele cells of wild-type hypocotyl explants initiated cell proliferation, giving rise to root primordia between day 1 and day 2. On day 2, adventitious root primordia reached the two-cell-layer stage. The root primordium formation of the rpd1-1 mutant proceeded normally until this stage. However, after 3 d of culture, developmental defects became evident in the mutant. On day 3, the wild-type primordium continued to develop, becoming hemispherical. In the rpd1-1 mutant, however, the development of the root primordium was arrested or strongly retarded at the two- to four-cell-layer stages. Therefore, the rpd1 mutation inhibited the development of adventitious root primordia beyond the two-cell-layer stage without affecting the earlier processes of primordium development, including the initiation of cell proliferation.
Because the hypocotyl segments used in the above experiments were excised from seedlings that had been grown at the permissive temperature (22°C), the normal development of root primordia at the very initial stage in the rpd1-1 explants cultured at 28°C might be attributable to the remnant of the RPD1 function active at 22°C. To test this possibility, we examined the temperature sensitivity of adventitious root formation using hypocotyl segments excised from seedlings that had been exposed to 28°C for the 4 d before tissue culture, which was expected to eliminate residual RPD1 activity. In this experiment, cell proliferation was initiated normally in the rpd1-1 explants in culture on RIM at either 22°C or 28°C (data not shown). This result corroborates the proposition that the RPD1 function is not required for the initiation of cell proliferation.
To estimate the critical period for RPD1 activity during adventitious root formation, we performed temperature-shift experiments with rpd1-1 (Fig. 2). Hypocotyl explants of the wild-type and rpd1-1 mutant were cultured at 22°C for 1 to 3 d, after which the temperature was shifted up to 28°C. After a total 6 d in culture, the explants were examined for adventitious rooting phenotypes. When the temperature was maintained at 28°C throughout the culture (Fig. 2K) or shifted up on day 1 (Fig. 2J), the adventitious roots of the rpd1-1 explants showed developmental arrest at the primordial stage. In contrast, when the temperature was shifted up at day 3, all the rpd1-1 explants formed normal adventitious roots (Fig. 2H), as occurred in culture at 22°C (Fig. 2G). A temperature shift on day 2 induced variable phenotypes among the rpd1-1 explants, but about half of them formed normal adventitious roots (Fig. 2I). This indicates that 2 d of culture at 22°C is sufficient for subpopulation of rpd1-1 hypocotyl explants to complete adventitious root formation. As no cell proliferation was recognizable in any of the hypocotyl explants before temperature shift in this condition (Fig. 1), this suggests that RPD1 is required during the limited period before cell proliferation becomes visible.
When rpd1-1 explants were grown at 28°C for 3 d, after which the temperature was shifted down to 22°C, they formed adventitious roots that were not morphologically different from those of the wild-type explants (Fig. 2L). Therefore, the defect caused by the rpd1 mutation is reversible, and the rpd1 root primordia were readily released from developmental arrest by a temperature shift from 28°C to 22°C.
During the early phase of root primordium development, auxin accumulates within the root primordium. An auxin gradient with the maximum at the primordium tip is then gradually established, which is considered to play an important role in the further development of the root primordium (Benková et al., 2003
In the wild-type explants, DR5:GUS activity became detectable in association with the initiation of adventitious root primordia by day 2 (Fig. 3A). Thereafter, the GUS activity increased around the primordial tip, and a steep gradient was evident within the root primordium on day 4. This gradient of GUS activity was also established in the adventitious root primordium of the rpd1-1 mutant at days 3 and 4, but it was much more broadly localized than in the wild-type primordium. The altered pattern of DR5:GUS expression in the rpd1-1 primordium appeared to correlate with the developmental arrest of the primordium. Before the defect in the rpd1-1 primordium was morphologically detectable, however, no obvious difference in DR5:GUS expression was observed between the wild type and rpd1-1. These results suggest that the rpd1 mutation does not primarily affect auxin accumulation patterns.
END199 is a SCARECROW (SCR) reporter line in which the uidA gene is inserted in the promoter region of the SCR gene. In this line, GUS activity is expressed under the control of the SCR promoter specifically in the endodermis, endodermis/cortex initials, and the quiescent center of mature roots (Malamy and Benfey, 1997
The effect of the rpd1 mutation on the activity of the root apical meristem was examined by monitoring the growth rates of primary roots. When rpd1-1 seedlings were first grown at 22°C and the temperature was then shifted up to 28°C, the growth rate decreased with a time lag of about 2 d after the temperature shift. It then dropped to zero within the next 3 d (Fig. 4). This result demonstrates that the rpd1 mutation interferes with the maintenance of meristematic activity, as well as with the development of the root primordium.
Effect of the rpd1 Mutation on Callus Formation Hypocotyl explants of the rpd1-1 mutant were cultured on callus-inducing medium at 22°C or 28°C, and time course of callus formation was compared with that in the wild-type explants (Fig. 5). In the rpd1 explants cultured at 28°C, callus formation started at the same time as in the wild-type explants. During the first 4 d of culture, callus growth appeared not to be affected by the rpd1 mutation. After day 4, however, callus growth in the rpd1 explants was retarded severely at 28°C. Thus the rpd1 mutation inhibited not the initiation but the maintenance of callus cell proliferation.
Cloning of the RPD1 Gene The rpd1-1 mutation was mapped within a 110-kb region at the 83-cM position of chromosome IV (Fig. 6A). Sequence analysis of genomic DNA in this region revealed that both rpd1-1 and rpd1-2 have a nucleotide substitution in At4g33495. A genomic fragment encompassing At4g33495 complemented the adventitious rooting phenotype of rpd1-1 at 28°C (data not shown). From these results, we concluded that At4g33495 corresponds to the RPD1 gene.
Determination of the cDNA sequence of RPD1 and its comparison with the genomic sequence showed that the RPD1 gene is composed of two exons and one intron. The intron is located downstream from the stop codon (data not shown). The predicted RPD1 protein consists of 409 amino acid residues. RPD1 shows no homology with any proteins of known function. A database search detected several sequences related to RPD1 among the expressed sequence tags (ESTs) of various plants, including the fern, Ceratopteris richardii (accession nos. BE643047 and BE643199), and the moss, Physcomitrella patens (BJ954318), but no such sequences were found of algal, animal, fungal, or bacterial origin (data not shown). In the Arabidopsis genome, there are 13 annotated genes and one EST encoding RPD1-like proteins (Fig. 6B). RPD1 and RPD1-like proteins share similarities throughout their sequences, except for the amino- and carboxy-terminal extensions (Fig. 6B). They are annotated to localize in mitochondrion or plastid except for At3g63090, although RPD1 and some of RPD1-like proteins have putative nuclear localization signals according to analysis with the PSORT prediction software (http://psort.ims.u-tokyo.ac.jp/; Fig. 6B).
Expression profiles of the RPD1 gene were analyzed by semiquantitative reverse transcription (RT)-PCR (Fig. 7). RPD1 mRNA was expressed in all organs of 14-d-old seedlings (Fig. 7A). It was relatively abundant in the shoot apex and the root. In hypocotyl explants induced to form adventitious roots, RPD1 expression showed a 2- to 3-fold increase in the first 12 h of culture at either 22°C or 28°C (Fig. 7B). This was at least 1 d earlier than the first sign of adventitious root initiation detectable microscopically (Fig. 1).
As the sole intron of RPD1 is more than 360 bases distant from the rpd1-1 and rpd1-2 mutations, its splicing does not seem to be influenced by these mutations. In support of this, RT-PCR analysis indicated accumulation of the normally spliced RPD1 mRNA in the rpd1-1 explants cultured at 28°C at a similar level to that found in the wild type (data not shown).
Two lines that harbor T-DNA insertions in the RPD1 gene were identified in the collection of SALK T-DNA insertion lines (Alonso et al., 2003 The T4 population was produced from each T3 plant heterozygous for the rpd1-3 mutation through self reproduction. The T4 individuals were genotyped with respect to the T-DNA insert and the RPD1 gene. All the T4 individuals had the intact RPD1 gene, and two thirds of them had the T-DNA insertion (Table I), suggesting that homozygotes for the rpd1-3 mutation are embryo lethal. Introduction of the genomic fragment containing At4g33495, namely RPD1 into the RPD1/rpd1-3 heterozygotes resulted in the recovery of progeny homozygous for the rpd1-3 mutation in the presence of a transgene-derived copy of RPD1. This demonstrated that the embryo lethality in the rpd1-3 lines was caused by the knockout of the RPD1 gene.
T4 plants genotyped as RPD1/rpd1-3 were indistinguishable in morphology and growth from RPD1/RPD1 plants of the same population (data not shown). However, heterozygous T4 plants produced both green and white seeds by self reproduction (Fig. 8A). In their mature siliques, embryos at the globular or transition stages were observed together with bent-cotyledon stage embryos (Fig. 8, C and D). The overall morphology of the arrested embryos appeared normal (Fig. 8E).
To gain information about effects of disruption of RPD1-related genes on embryogenesis, we searched the database of SeedGenes project (http://www.seedgenes.org/; Tzafrir et al., 2004 ) and found one RPD1-related gene, At5g62990/EMB1692. According to the presented information, T-DNA insertion in At5g62990/EMB1692 causes embryogenesis arrest at the transition stage, which is similar to the case of the RPD1 knockout line.
We characterized in silico the two conserved regions of RPD1 and RPD1-like proteins where the rpd1-1 and rpd1-2 mutations reside, and noticed that they are structurally related to each other (Fig. 9). These regions are designated domain A (residues 139–216 of RPD1) and domain B (residues 285–362 of RPD1).
As shown in Figure 9B, domains A and B share low but significant sequence similarity. Higher structures of these domains were compared using the three-dimensional position-specific scoring matrix (3D-PSSM) system (Kelly et al., 2000 ; http://www.sbg.bio.ic.ac.uk/ 3dpssm/), which returns secondary structure predictions based on the PSI-Pred program (Jones, 1999), in addition to the top 20 hits of potentially structurally related proteins. The secondary structures of domains A and B were predicted to be H-short S-H-H-S-S and H-H-H-S-S, respectively (H for  helix and S for strand; Fig. 9B). Thus domains A and B are very similar in their overall secondary structures. Searches of 3D-PSSM with domains A and B as queries hit various helical proteins. Proteins that belong to the winged helix superfamily were most frequently found in the search results for both domains A and B. Winged helix consists of three helices, three strands, and two extended loops (wings; W) that are arranged in the order of H1-S1-H2-turn-H3-S1-W1-S2-W2 (Gajiwala and Burley, 2000). Alignment of the sequences of RPD1 and RPD1-like proteins with those of winged helix proteins indicated that conserved hydrophobic residues in domains A and B are located at the position of the hydrophobic core of winged helix proteins (Fig. 9, B and C; Clark et al., 1993; Gajiwala and Burley, 2000; Okuda et al., 2000; Schwartz et al., 2001). These results suggested a possible relationship of RPD1 and RPD1-like proteins with winged helix proteins. Sequence comparison of RPD1 and RPD1-like proteins also detected three 6-amino acid motifs, K/RH/YPXXF (X denotes arbitrary amino acid; Figs. 6B and 9A). Domain A and domain B contain the second and the third K/RH/YPXXF motifs, respectively. The last residue Phe of each K/RH/YPXXF motif is completely conserved among RPD1-related proteins, suggesting its importance in this group of proteins.
RPD1 Is Required for the Maintenance of Active Cell Proliferation The rpd1 mutants (rpd1-1 and rpd1-2) were initially characterized by their temperature-sensitive development of adventitious root primordia. In this study, we further analyzed the adventitious rooting phenotype of rpd1, taking advantage of its temperature sensitivity. Microscopic observation of the time course of adventitious root formation at the restrictive temperature showed that the rpd1 mutation does not affect the initial phase of development of adventitious root primordia, but retards their development beyond the two- to four-cell-layer stages (Fig. 1). Temperature-shift experiments localized the window of requirement for the RPD1 function to the period before cell proliferation becomes recognizable (Fig. 2). These findings suggest that the RPD1 function is related to stage-specific events involved in root primordium development, rather than to fundamentals required throughout organogenesis.
During the early development of root primordia, establishment of the apical-basal axis and cellular organization occur in correlation with changes in auxin accumulation patterns (Malamy and Benfey, 1997
The other notable feature of root primordium development is a rapid increase in cell number (MacLeod and Thompson, 1979
As discussed above, the rpd1 mutations caused apparently stage-specific defects in root primordium development. However, in the apical growth that depends on meristematic activity, the effects of the rpd1 mutations seem to be cumulative. For example, exposure of the rpd1-1 mutant to the restrictive temperature did not halt primary root growth immediately, but decreased the growth rate gradually after a time lag of about 2 d (Fig. 4). These differential effects of the rpd1 mutations might reflect differences in cell-cycle duration. Estimates of 5 to 9 h have been reported for cell-cycle duration during the development of lateral root primordia and embryos in Arabidopsis (Bowman and Mansfield, 1994 In summary, the RPD1 gene is inferred to have an important function in maintaining active cell proliferation, particularly when the cell-division cycle is very rapid. It should be noted again that the initial stages of adventitious root development and callus formation are quite normal in the rpd1-1 explants, even at the restrictive temperature. Therefore, we could say that the RPD1 function is required for the maintenance of active cell proliferation, but not for the reactivation of the cell cycle in quiescent cells or the progression of every cycle of cell division.
RPD1 encodes a member of a novel protein family (Fig. 6). Database searches detected many sequences encoding RPD1-like proteins in ESTs of various plants, including monocots, a fern, and a moss. However, no related proteins were found in algae, animals, fungi, or bacteria. Therefore, this protein family is specific to plants. It is of interest to resolve how and when the RPD1 family originated in the history of plant evolution.
RPD1 and related proteins contain no known domains or motifs, except the putative transit peptide and nuclear localization signal. However, careful comparison of the sequences of these proteins and 3D-PSSM search led to the identification of two domains representing a large repeat conserved among RPD1-related proteins (Fig. 9). The rpd1-2 and rpd1-1 mutations occur in the first and second domains, respectively, suggesting that these domains are important for the function of RPD1. It is notable that these domains might be structurally related to the winged helix proteins, which are involved in various regulatory functions through DNA binding, RNA binding, or protein-protein interaction (Clark et al., 1993
Plant Materials
Of two rpd1 mutants (rpd1-1 and rpd1-2) of the ecotype Landsberg erecta (Ler) origin, we used rpd1-1 as a representative of the rpd1 mutant in this study, unless otherwise indicated. An auxin-responsive reporter line of the Columbia origin carrying DR5:GUS (Ulmasov et al., 1997
Tissue culture experiments were performed as described by Konishi and Sugiyama (2003)
Hypocotyl explants were fixed at 4°C in a 9:1 mixture of ethanol and acetic acid, hydrated through a graded series of ethanol, and mounted with a drop of clearing solution (a mixture of 8 g chloral hydrate, 2 mL water, and 1 mL glycerol). Cleared samples were observed under a light microscope equipped with Nomarski optics (BX50-DIC; Olympus).
Hypocotyl explants were fixed in 90% acetone at –20°C overnight and rinsed three times with 0.1 M sodium phosphate buffer (pH 7.4). They were incubated in X-Glc solution (0.5 mg/mL 5-bromo-4-chloro-3-indolyl-
Seeds were surface sterilized and sown on germination medium A (GMA). GMA is Murashige and Skoog medium (Murashige and Skoog, 1962
Chromosome mapping was performed according to the standard procedure as described previously (Konishi and Sugiyama, 2003
Genomic DNA was extracted from the wild-type (Ler) and the rpd1 mutants with Isoplant II (Nippon Gene), and subjected to PCR amplification with gene-specific primer sets. The PCR product was treated with ExoSAP-IT (USB) and used as the template for cycle sequence reactions with BigDye Terminator Cycle Sequencing FS Ready Reaction kit (Applied Biosystems), according to the manufacturer's protocol. Sequencing was carried out with an ABI PRISM 377 DNA sequencer (Applied Biosystems). The sequence data were analyzed with Genetyx-Mac software version 10 (Genetyx).
Total RNA was extracted from Ler hypocotyl explants that had been cultured on RIM for 1 d at 28°C and used as the template for the first-strand cDNA synthesis. cDNA synthesis and its amplification by nested PCR were performed with the SMART RACE cDNA amplification kit (BD Biosciences). The RPD1-specific primers used were: 5'-GSP (5'-AAGCCGAGACCTAGACGACGAGCGAGCG-3') and 5'-GSP2 (5'-CTGTGAAATTTGACGACTTTGCGG-3') to amplify the 5' end of RPD1 cDNA; and 3'-GSP (5'-CGAGGAAATTACGGGAAGCTTCATACGG-3') and 3'-GSP2 (5'-AAGAGAGGGGAATTGGTAGAACCG-3') to amplify the 3' end. The amplified DNA fragments were cloned into the pGEM-T Easy Vector (Promega) and subjected to sequence analysis.
The genomic clone GL3631, which was used for the complementation test, was isolated from our transformation-competent genomic library. In this library, genomic fragments of Ler were inserted into the pNH01 binary vector, which had been constructed from pIG121-Hm (Akama et al., 1992
A simplified version of the floral dip method was used for plant transformation (Clough and Bent, 1998
RNA extraction was carried out as described by Ozeki et al. (1990)
Insertion mutant information was obtained from the SIGnAL Web site at http://signal.salk.edu. For knockout analysis of the RPD1 gene, T3 plants heterozygous for the T-DNA insertion were selected by PCR-based screening of the SALK lines, SALK_123424 and SALK_123464. The presence of the RPD1-inserted T-DNA was checked by PCR amplification of it with a RPD1-specific primer and the LBb1 primer (http://signal.salk.edu/). The PCR product was sequenced to confirm the site of T-DNA insertion. The presence of the intact RPD1 gene was checked by PCR amplification with RPD1-specific primer sets. T4 lines obtained by self reproduction of each T3 plant were used for genotypic and phenotypic analyses. For complementation analysis, the genomic fragment of the Ler origin containing RPD1 was introduced into plants heterozygous for the T-DNA insertion (Columbia background) via the transformation-competent genomic clone GL3631, and the resultant transformants were genotyped. The GL3631-derived copy of RPD1 (Ler origin) and the endogenous RPD1 (Columbia origin) were distinguished using a new CAPS marker, which was developed for a flanking single nucleotide polymorphism (residue 16113626 of chromosome IV) between Ler and Columbia. The nucleotide sequence of RPD1 mRNA of Ler origin has been deposited with the DNA Data Bank of Japan/EMBL/GenBank databases under accession number AB189464.
We thank Dr. Tom. J. Guilfoyle (University of Missouri) for the generous gift of the DR5:GUS line seeds, Drs. Philip N. Benfey (New York University) and Hidehiro Fukaki (Nara Institute of Science and Technology) for the END199 seeds, and the Salk Institute Genomic Analysis Laboratory for providing the sequence-indexed Arabidopsis T-DNA insertion mutants. Received November 26, 2005; returned for revision November 26, 2005; accepted December 19, 2005.
1 This work was supported by Grants-in-Aid from the Ministry of Education, Sports, Culture, Science and Technology of Japan (RFTF00L01605 and no.14036209). Funding for the SIGnAL indexed insertion mutant collection was provided by the National Science Foundation. 
2 Present address: Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113–8657, Japan. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Munetaka Sugiyama (sugiyama{at}ns.bg.s.u-tokyo.ac.jp). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.074724. * Corresponding author; e-mail sugiyama{at}ns.bg.s.u-tokyo.ac.jp; fax 081–3–3814–0139.
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TOP
ABSTRACT
RESULTS
, Swissprot accession