Journal of Experimental Botany, Vol. 51, No. 352, pp. 1789-1797,
November 1, 2000
© 2000 Oxford University Press
Original Papers |
Isolation of three distinct CycD3 genes expressed during fruit development in tomato1
The Horticulture and Food Research Institute of New Zealand Ltd., Mt. Albert Research Centre, Private Bag 92169, Auckland, New Zealand
Received 7 March 2000; Accepted 26 June 2000
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Abstract |
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Tomato (Lycopersicon esculentum Mill.) is an important fruit crop world-wide and a model for studying fruit development. As determined using flow cytometry, fruit growth was characterized by high cell division activity in tomato during the first week after anthesis and followed by endoreduplications (DNA replication without cell divisions). D-type cyclins are considered to be important parts of the signal transduction for stimulation of DNA replication and cell division. To study the function of D cyclins in fruit development, full-length cDNA clones for three D cyclin genes were isolated from young tomato fruit. They were classified as D3 cyclins by sequence similarities and a phylogenetic analysis and named as LeCycD3;1, LeCycD3;2 and LeCycD3;3. The deduced amino acid sequences for LeCycD3;1–3 contained a retinoblastoma-binding motif and a PEST-destruction motif. Pollination and fertilization were followed by a high increase in the transcript levels of LeCycD3;1–3 in young fruit. Using in situ hybridization, high expression of LeCycD3;3 was detected in the vascular tissue of young fruit suggesting a role in vascular development. The D3 cyclins are probably involved in transducing the signals leading to fruit growth by cell divisions. Distinct differences were detected in their temporal and spatial expression patterns suggesting that they play different roles in fruit development as well as in the development of other plant organs.
Key words: Cell cycle, cyclin, fruit development, Lycopersicon esculentum.
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Introduction |
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The growth of a fruit after anthesis starts by stimulation of cell divisions in the tissues forming the fruit flesh (reviewed by Coombe, 1976
). The cell division activity is usually restricted to an initial period of a few weeks after anthesis, followed by cell expansions that make the greatest contribution to the final fruit size. In tomato (Lycopersicon esculentum Mill.), pollination and fertilization stimulate cell divisions in the ovary and these continue for approximately 7–10 d (reviewed by Gillaspy et al., 1993). Throughout the development of tomato fruit, there are repeated cycles of DNA synthesis without intervening cell divisions (endoreduplications) in the pericarp resulting in endopolyploid cells (Bergervoet et al., 1996; Joubès et al., 1999). Endopolyploidy is very common in differentiated plant cells (reviewed by Traas et al., 1998), including tomato (Smulders et al., 1994), and has been found to be closely linked to differentiation and cell expansion.
Complexes containing cyclins and cyclin-dependent protein kinases (CDK) play a central role in the regulation of cell-cycle progression in eukaryotes such as yeast (reviewed by Forsburg and Nurse, 1991; Nasmyth, 1996) and animals (reviewed by Norbury and Nurse, 1992). The binding of cyclin to the CDK is necessary for protein kinase activity and for determining target specificity (Morgan, 1995; Nigg, 1995). The cyclins share the presence of the relatively conserved cyclin box of about 100 amino acids, which is responsible for CDK binding and activation, and they are classified according to sequence identities and activity during the cell cycle. Many cyclins are used to control different stages of cell-cycle progression and oscillating gene transcription and protein breakdown mainly controls their activity. In animals, mitotic A- and B-type cyclins are needed for progression through G2 and for mitosis. In addition, cyclin A is essential for S phase. Important regulators of G1 progression and G1 to S transition are the cyclins D1, D2, D3, and E (Sherr, 1993, 1994). D-type cyclins induce CDK activity after stimulation by growth factors and transduce extracellular signals for stimulation of cell division.
Over 60 cyclin cDNA clones have been isolated from a number of plants (reviewed by Renaudin et al., 1996). Most of these are related to the mitotic A- and B-type cyclins. The G1 cyclins are less conserved than the mitotic cyclins and complementation of yeast G1 cyclin mutants were initially used to isolate three D cyclins from Arabidopsis (Soni et al., 1995) and one from Medicago sativa (Dahl et al., 1995). These plant sequences have recently been utilized for the isolation of D cyclin clones from pea (Shimizu and Mori, 1998), tobacco (Sorrell et al., 1999) and Chenopodium (Fountain et al., 1999). A D-type cyclin has also been isolated through its interaction with Cdc2 in a two-hybrid screen (De Veylder et al., 1999). In agreement with the hypothesis that plant D cyclins are involved in transducing growth signals into the cell cycle, Arabidopsis CycD3 seems to transduce the cytokinin activation of the cell cycle at the G1–S transition (Riou-Khamlichi et al., 1999), and Arabidopsis CycD2 and CycD4 expression is induced by carbon source (Fuerst et al., 1996; De Veylder et al., 1999). Plant D cyclins have been shown to be able to bind retinoblastoma-related proteins (Ach et al., 1997; Huntley et al., 1998; Nakagami et al., 1999) and also together with Cdc2 phosphorylate a Rb-related protein (Nakagami et al., 1999). This suggests that plant D cyclins may act in the control of G1–S by phosphorylation of Rb-related proteins as previously shown in animals.
The important connection between plant development and cell division/cell expansion is very complex and poorly understood (see for example Hemerly et al., 1999). To understand better the molecular regulation of the cell division and cell expansion phases of fruit development, full-length clones for three D3 cyclin genes from tomato have been isolated and characterized increasing the number of known D3 cyclins in plants. These results suggest that the three D3 cyclin genes have different functions in plant development and show that they are expressed during both the cell division and cell expansion/endoreduplication phases of fruit development.
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Materials and methods |
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Plant material
Tomato plants (Lycopersicon esculentum Mill., cv. UC82B) were grown under greenhouse conditions. Flowers were tagged at anthesis and the fruit collected at specific time points after anthesis.
PCR amplification of cyclin gene fragments
To isolate cyclin D3 cDNA from tomato, two degenerate PCR primers were designed based on the sequences VNAHYGF and KYVFEAK of the cyclin box. These regions are strictly conserved between cyclin D3 from Arabidopsis thaliana (Soni et al., 1995) and cycMs4 from Medicago sativa (Dahl et al., 1995).
The primers, fwd: 5' TGTGTTGTCGAC/GT(C/G/T) AA (C/T)GC(A/C/T)CA(C/T)TA(C/T)GG(A/C/G/T)TT 3' rev: 5' TGTGTTGCGGCCGC/TT(A/G/T)GC(C/T)TC(A/G) AA(A/G/C)AC(A/G)TA(C/T)TT 3', are 288- and 144-fold degenerate, respectively. Restriction sites for Sal I and Not I were included in the primers to facilitate cloning. Double-stranded cDNA (1 ng) from young tomato fruit was used as template for the PCR, which consisted of initial denaturing (5 min at 94 °C), 5 cycles (1 min at 94 °C, 2 min at 42 °C, and 3 min at 72 °C), 30 cycles (1 min at 94 °C, 1 min at 50 °C and 3 min at 72 °C) and a final extension of 7 min at 72 °C. The obtained fragments were cloned into Bluescript SK (+/-) (Stratagene, La Jolla, CA, USA).
To isolate a partial cyclin B1 cDNA from tomato, primers based on Ntcyc29 (Nicta;CycB1;2) from Nicotiana tabacum (Setiady et al., 1995) were used. The primers, fwd: 5' TGT-GTTGTCGACGCTAGGAGCAAGGCTGCCTG 3' and rev: 5' TGTGTTGCGGCCGCTAAGGTGTTGGGACTGTTAA 3', were designed to amplify a fragment corresponding to bp 412–911 of Ntcyc29. Restriction sites for Sal I and Not I were included in the primers to facilitate cloning. Double-stranded cDNA (2 ng) from young tomato fruit was used as template for the PCR, which consisted of initial denaturing (4 min at 94 °C), 5 cycles (1 min at 94 °C, 1 min at 50 °C and 2 min at 72 °C), 30 cycles (1 min at 94 °C, 1 min at 54 °C and 2 min at 72 °C) and a final extension of 7 min at 72 °C.
cDNA library construction and screening
Total RNA was isolated from 0–7-d-old tomato fruit using TRIZOL reagent (Life Technologies, Gaithersburg, MD, USA). Poly(A)+ RNA was enriched by two rounds of column purification (mRNA Purification Kit, Pharmacia, Uppsala, Sweden). A cDNA library was constructed in 
Uni-ZAP XR vector as described in the instruction manual (Stratagene). 2x105 phage colonies were screened on Hybond-N+ filters (Amersham, England) by standard procedures (Sambrook et al., 1989). A 32P-labelled probe was generated from the cloned D-cyclin fragment by random priming using the RTS RadPrime DNA Labeling System (Life Technologies). DNA inserts from positive clones were excised according to the protocol from the manufacturer.
Southern blot analysis
Genomic DNA was isolated from leaves of tomato, tobacco (Nicotiana tabacum) or petunia (Petunia hybrida) using minor modifications of the CTAB protocol (Doyle and Doyle, 1990). 10 µg of DNA was digested with the appropriate restriction enzymes, subjected to electrophoresis in a 0.8% agarose gel, transferred to a Nytran Plus nylon filter (Schleicher and Schuell, Dassel, Germany) and hybridized at 65 °C according to standard procedures (Sambrook et al., 1989). Probes were prepared by isolation of fragments from plasmid clones and 32P-labelled as described above. The filters were washed twice for 10 min with 2x SSC (1x SSC: 0.15 M NaCl, 15 mM trisodium citrate, pH 7.0), 0.1% sodium dodecyl sulphate (SDS) at 65 °C; and finally for 20 min with 2x SSC, 0.1% SDS (low stringency), or 0.5x SSC, 0.1% SDS (high stringency) at 65 °C. The filters were exposed to X-ray film (Kodak X-OMAT AR) between intensifying screens or analysed by a PhosphorImager (Molecular Dynamics, Sunnyvale, CA, USA).
Northern blot analysis
Tomato fruit was harvested at defined time points after anthesis. Plant material was frozen in liquid nitrogen and used immediately or stored at -70 °C. Total RNA from tomato vegetative parts, flowers and fruit up to 2 weeks after anthesis was isolated using TRIZOL reagent. Another method was used to isolate total RNA from 3- and 6-week-old fruit (López-Gómez and Gómez-Lim, 1992). Total RNA (10 or 20 µg per sample) was subjected to electrophoresis in formaldehyde-agarose gels and transferred to Nytran Plus nylon filters (Schleicher and Schuell) according to standard procedures (Sambrook et al., 1989). Hybridization of the Northern blot filters was performed as described above for the Southern blot filters. Hybridization signals were quantified from the blots using a PhosphorImager (Molecular Dynamics). The amount of RNA in each sample was determined by hybridization of the filters with an apple 18S rRNA probe (Simon and Weeden, 1992). The quantified data were equalized by normalizing to the amount of rRNA.
In situ hybridization
Tomato fruit at 6 d after anthesis and flower peduncle were fixed and embedded. The methods used for digoxigenin labelling of RNA probes, tissue preparation and in situ hybridization were mainly as described in Jackson (Jackson, 1992). The probe region was the same as for the northern and Southern blot hybridizations. The LeCycD3;3 probe consisted of bp 1–1149.
Sequence analysis
DNA sequences were determined by the dideoxynucleotide method with dye terminators on an Applied Biosystems 373 DNA sequencer (University of Auckland, New Zealand). The complete sequences of full-length clones were determined on both strands by generation of deletions with restriction enzymes or by use of synthetic oligonucleotides. DNA sequence data were assembled and analysed with the GCG package (version 9; Genetics Computer Group, Madison, WI). Multiple sequence alignments for phylogenetic analysis were produced using CLUSTAL W 1.74. Parsimony analysis was accomplished using PAUP 3.1s (Swofford, 1993). Gaps were treated as missing data. Possible PEST-destruction sequences were identified using the PEST-find programme (Rechsteiner and Rogers, 1996).
Flow cytometry
Nuclei from tomato fruit cells were isolated and prepared as described before (O'Brien et al., 1996). The relative DNA content was determined by cytometric analysis using an EPICS Elite ESP flow cytometer (Coulter Electronics, Hialeah, Florida, USA) with the 488 nm line of an argon laser. For each sample the DNA content of at least 10 000 nuclei was determined.
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Results |
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Cell divisions and endoreduplications follow induction of fruit growth
To characterize the cell division activity during early fruit development, the nuclear DNA contents were determined in young fruit of the tomato cultivar UC82B using flow cytometry (Fig. 1
). At anthesis diploid cells dominated in the ovary, with only a low level of DNA replication activity (visible as the cells between 2C and 4C). However, by day eight after anthesis (8 DPA) a population of 8C cells was observed together with a high level of DNA replication, and at 20 DPA few 2C cells remained in favour of populations of 4C, 8C and 16C cells. This shows that during early fruit development there is a short initial phase of cell divisions followed by a high activity of endoreduplications. Similar results were obtained for the cherry tomato cultivar VFNT (not shown).
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Isolation of tomato cDNA for D3 cyclins
A DNA fragment of 243 bp was produced by PCR of cDNA from young tomato fruit, and the deduced amino acid sequence of the fragment showed high similarity to plant D3 cyclins. The cloned PCR fragment was used to screen a library corresponding to the same tissue, and three different cyclin genes were identified among 160 positive clones: Lyces;CycD3;1 (or LeCycD3;1), Lyces;CycD3;2 (or LeCycD3;2) and Lyces;CycD3;3 (or LeCycD3;3). The initial PCR fragment was completely identical to part of LeCycD3;2. The inserts of the longest clones for LeCycD3;1, LeCycD3;2 and LeCycD3;3 were 1518 bp, 1460 and 1449 bp in length, respectively, and contained open reading frames encoding putative proteins with 359, 364 and 336 amino acids (Fig. 2). In-frame stop codons were present upstream of the first methionine codons in all cases indicating that these clones contain the full coding sequences. The deduced amino acid sequences of LeCycD3;1–3 had similar predicted molecular weight, around 40 000, with a predicted pI of around 4.8. Alternative poly-adenylation sites were detected for LeCycD3;1 and LeCycD3;2 (not shown).
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The predicted amino acid sequences of the tomato cyclins were 47–51% identical to each other over the entire length, 48–61% to the published D3 cyclins from Arabidopsis and alfalfa, and 28–31% to Arabidopsis CycD2 and CycD1. Besides the presence of a cyclin box, the predicted proteins of LeCycD3;1–3 displayed two characteristic structural elements of D cyclins. Firstly, the motif LxCxE, which binds to retinoblastoma-related proteins (Sherr, 1993
; Renaudin et al., 1996), was present in the N-terminals (Fig. 2
), and secondly, possible PEST regions were detected at identical positions in the C-terminus of all three tomato cyclins (Fig. 2). G1 cyclins are rapidly turned over and the proteolytic degradation is dependent on PEST regions (reviewed by Rechsteiner and Rogers, 1996). The destruction of mitotic cyclins is conferred by a partially conserved ‘destruction box’, RxALGxIxN, in the N-terminal domain (Glotzer et al., 1991). Similar to other D cyclins, no parts of the LeCycD3 sequences showed any similarity to the destruction box.
Phylogeny and genome organization of D3 cyclin genes
A phylogenetic analysis based on the amino acid sequences of cyclin boxes (corresponding to amino acid 89 to 194 in LeCycD3;1) confirmed their identity as D3 cyclins (Fig. 3a), and showed that the D cyclins from plants, animals and yeast have a common origin separate from the A- and B-cyclins. The monophyletic origin of plant D cyclins also showed that the diversification of D cyclin families in plants, animals and yeast has occurred independently. A phylogenetic analysis using the complete amino acid sequences of plant D3 cyclins strongly suggested that tomato LeCycD3;1 and tobacco NtCycD3;2, and tomato LeCycD3;2 and tobacco NtCycD3;1 are orthologues (Fig. 3b).
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Southern blot experiments showed that the three D3 cyclin genes are present as single copy genes in the tomato genome, while a LeCycD3;1 probe containing the conserved cyclin box detected approximately four genes at low stringency (not shown).
Differential expression of D3 cyclin genes during plant development
High expression levels of the three D3 cyclins, and a histone H4 gene as a marker for DNA replication (Brandstädter et al., 1994), were detected in tissues containing dividing cells, such as vegetative buds, flower buds, young fruit, young roots, and young leaves (Fig. 4). Transcripts for LeCycD3;1–3 and histone H4 were also observed in seedlings and mature leaves. The relative abundance of transcripts in different tissues varied between the D3 cyclin genes. LeCycD3;2 and histone H4 were equally highly expressed in vegetative shoots, flower buds, young fruit, and young leaves, while LeCycD3;1 was preferentially expressed in young fruit, and LeCycD3;3 at lower levels in fruit compared with vegetative shoots, flower buds and young leaves. The different expression patterns of the three D cyclins suggest that they are developmentally regulated and that they have different roles in the control of cell-cycle progression. The transcript size of 1.5 kb for LeCycD3;1–3 corresponded well with those of the clone inserts.
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The expression of D3 cyclin genes is up-regulated after fertilization
The expression of LeCycD3;1–3, a tomato B1 cyclin homologue (Lyces;CycB1;1 or LeCycB1;1), and histone H4 was rapidly stimulated in ovaries after pollination/fertilization (Fig. 5). As soon as 1 d after anthesis (1 DPA), the transcript levels of LeCycD3;1, LeCycD3;2 and histone H4 had increased significantly. The transcript levels of the D3 cyclin genes, the B1 cyclin gene, as well as that of histone H4, peaked at 3 DPA, then gradually decreased but was still easily detectable at 14 DPA. The expression of LeCycD3;1–3 and histone H4 was still detectable at 3 weeks after anthesis in whole fruit and in the pericarp (not shown). After prolonged exposure, expression of all D3 cyclin genes could also be observed at the breaker stage of fruit development 6 weeks after anthesis. There were distinct differences in the expression levels of the three D-cyclin genes in ovaries and young fruit. The transcript levels of LeCycD3;1, similar to LeCycB1;1 and histone H4, were stimulated by fruit set, with a more than a 5-fold difference from anthesis to 3 DPA. LeCycD3;3 transcripts were abundant pre-anthesis, dropped to anthesis, were slowly stimulated by fruit set and then decreased to a low level. The LeCycD3;2 transcript level was more constant with a 3-fold increase from anthesis to 3 DPA.
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In contrast, the tomato homologue of 21D7 nuclear antigen from carrot, a putative 26S proteasome subunit (Smith et al., 1997
; A Kvarnheden et al., unpublished results), had a constant transcript level from anthesis to 2 weeks after anthesis.
Localization of cyclin expression
In situ hybridization was used to detect the localization of LeCycD3;3 expression in 6-d-old fruit. The results from the Northern blot experiments (Fig. 5) had shown that at this time point, the transcript levels of the D3 cyclin genes and the B1 cyclin gene were still elevated compared to anthesis, but had decreased from their peaks at 3 DPA. LeCycD3;3 showed a weak signal in the placenta proximal to the seeds (Fig. 6b), and a stronger hybridization in the vascular tissue of placenta and pericarp (Fig. 6b, c), and of flower peduncle (Fig. 6d). The signal appeared to be in parenchyma and companion cells, but not in xylem vessels.
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Discussion |
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cDNA clones have been isolated from young tomato fruit, representing three new genes with high similarity to previously isolated D3 cyclins from Arabidopsis (Soni et al., 1995
) and alfalfa (Dahl et al., 1995), and containing the cyclin box, retinoblastoma-binding motif and PEST-destruction sequence characteristic for D cyclins. This was the first time that more than two members for this gene family were isolated and characterized from a single plant species. A phylogenetic analysis of cyclin boxes from a range of cyclins confirmed that these three tomato genes can be classified as D3 cyclins and also showed that the D cyclins from plants, animals and yeast have a common origin. Among the D cyclins, plant D cyclins formed a monophyletic clade suggesting the diversification of the D cyclin gene family to have occurred after the split between the plant, fungal and animal lineages. The genome of the ancestral organizm may have contained a very limited number of G1- and mitotic cyclin genes, which independently have been duplicated in the different lineages during evolution.
These Southern blot experiments suggested that there were four gene copies for D3 cyclins in tomato. Data from tobacco and petunia showed that other Solanaceae species also contained these three CycD3 genes in two or more copies (not shown). A Southern blot analysis that has been performed with Arabidopsis (Soni et al., 1995) further supports the idea that there is a small family of D3 cyclin genes in dicotyledonous plants.
The tomato D3 cyclin genes, as histone H4, were expressed throughout the plant, but with a preference for tissues with high levels of cell division, such as vegetative buds, flower buds, young fruit, young roots, and young leaves. The comparison of transcript levels for LeCycD3;1–3 in a range of tissues and during early fruit development showed that they were differently regulated suggesting them to have different functions. As visible in the in situ hybridization experiments, LeCycD3;3 showed high transcript levels in vascular tissue of young fruit and flower peduncle. This may reflect a specific role in the development of vascular tissue similar to CycD4;1 of Arabidopsis (De Veylder et al., 1999). Different expression patterns have been detected for two D3 cyclins in Antirrhinum (Doonan, 1998), with one gene expressed in all proliferating cells in the shoot, and the other D3 cyclin gene expressed in a subset of proliferating cells, as well as in tobacco with differential accumulation during the cell cycle for two tobacco D3 cyclins (Sorrell et al., 1999). The level of redundancy between the different plant D3-type cyclins and their specific functions remains to be determined.
The temporary resting stage at anthesis is broken by pollination and fruit growth is started by an initial phase of high cell division activity directly followed by endoreduplications and cell expansion. As soon as 1 d after anthesis there was a significant increase in transcript levels of LeCycD3;1 and 2, as well as histone H4, indicating that pollination/fertilization induces a rapid stimulation of cell-cycle gene expression. Recently, also the transcripts of two CDK genes were found to accumulate during the early phase of cell division in tomato fruit (Joubès et al., 1999). The transcript levels for the three D3 cyclin genes, cyclin B1, and histone H4 peaked at 3 DPA coinciding with the period of intense cell division activity in the pericarp (Gillaspy et al., 1993).
Plant hormones are likely to be involved in triggering fruit set. Both gibberellins and cytokinins levels peak during fertilization (Gillaspy et al., 1993), and several gibberellin synthesis genes were shown to be upregulated in young fruit compared with temporal low levels during anthesis (Rebers et al., 1999). The cyclin genes may be involved in transducing the hormonal signals leading to fruit growth by cell divisions.
The continued expression of histone H4 and the cyclins in the later stages of fruit development may be because of a low level of cell division and/or because of an association with the detected endoreduplications. Histone H2A has earlier been observed to be expressed in both cells undergoing cell division and endoreduplication during tomato plant development (Koning et al., 1991).
The PEST sequences of the D3 cyclins suggests that they are targeted for ubiquitin-mediated destruction by the 26S proteosome. The 21D7 nuclear antigen from carrot has been demonstrated to be a part of the 26S proteosome and has been suggested to participate in the control of cell division by regulating the activity or specificity of the 26S proteosome (Smith et al., 1997). However, the transcript level of the tomato 21D7 gene homologue remained relatively constant during early fruit development showing no correlation with the transcript levels of the D3 cyclin genes or histone H4. The constant levels of 21D7 mRNA probably reflects the fact that it has more functions besides proteolysis of cell-cycle regulatory proteins or that its activity is regulated post-transcriptionally.
In summary, three members of the CycD3 family of tomato have been isolated and characterized. Previously, only two members of this gene family had been identified from a given plant species. The expression of these genes was correlated with tissues with high cell division activity. However, the three CycD3 genes were differentially expressed in different tissues and during plant development suggesting them to have different functions. Further studies are now needed to specify the possible functions of the D3 cyclins in the regulation of cell division, endoreduplication and even more widely in plant development.
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Acknowledgments |
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The authors thank J Brandstädter at Universität zu Köln for the kind gift of the tomato histone H4 clone, J Doonan for helpful discussions and J Valkonen for critical discussions and comments on the manuscript. Financial support for this work was obtained from the New Zealand Foundation of Research, Science and Technology (CO6817).
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Notes |
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1 The nucleotide sequence data reported appear in the EMBL, GenBank and DDBJ Nucleotide Sequence Databases under the accession numbers: Lyces;CycD3;1 (AJ002588), Lyces;CycD3;2 (AJ002589), Lyces;CycD3;3 (AJ002590), and Lyces;CycB1;1 (AJ011108).
2 To whom correspondence should be addressed at: Department of Plant Biology, Swedish University of Agricultural Sciences, Box 7080, 750 07 Uppsala, Sweden. Fax: +46 18 673392. E-mail: Anders.Kvarnheden{at}vbiol.slu.se
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