JXB Advance Access originally published online on March 3, 2003
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Journal of Experimental Botany, Vol. 54, No. 385, pp. 1245-1251,
April 1, 2003
© 2003 Oxford University Press
Expression of CycD3 is transiently increased by pollination and N-(2-chloro-4-pyridyl)-N'-phenylurea in ovaries of Lagenaria leucantha
Received 25 June 2002; Accepted 2 January 2003
1 Department of Horticulture, Zhejiang University, Huajiachi Campus Kaixuan Road 268, Hangzhou 310029, China
2 Biotechnology Institute, Zhejiang University, Huajiachi Campus Kaixuan Road 268, Hangzhou 310029, China
3 To whom correspondence should be addressed. Fax: +86 571 86049815. E-mail: yu{at}mail.hz.zj.cn
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Abstract |
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Lagenaria leucantha is an important vegetable crop and a potential model for the study of fruit development. To study the function of D cyclins in fruit development, full-length cDNA clones for two D cyclin genes were isolated from young ovaries of Lagenaria leucantha. They were classified as D3 cyclins by sequence similarities and phylogenetic analysis, and nominated LlCycD3;1 and LlCycD3;2, respectively. The deduced amino acid sequence of both LlCycD3 genes contained a retinoblastoma-binding motif and a PEST-destruction motif. Unpollinated ovaries failed to develop and eventually aborted. N-(2-chloro-4-pyridyl)-N'-phenylurea (CPPU) induced parthenocarpic fruit significantly larger than pollinated ones. In unpollinated ovaries, the expression of both LlCycD3 genes was abundant at anthesis and then suddenly decreased, concomitant with the cessation of cell division. Pollination/fertilization induced an activation of the cell cycle accompanied by a large increase in the transcript levels of LlCycD3;1 and LlCycD3;2 in young fruits. Treating ovaries with CPPU also reactivated cell division and transcription of CycD3 genes and the effect was more rapid and pronounced than after pollination/fertilization.
Key words: Cucurbitaceae, CycD3, cytokinin, fruit development, pollination.
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Introduction |
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The growth of an ovary, after anthesis, starts by cell division in the tissues forming the fruit flesh (Coombe, 1976). Cell division activity is usually restricted to an initial period of a few days after anthesis, followed by cell expansions that make the greatest contribution to the final fruit size. This growth of fruits is triggered by fertilization in seed plants and is associated with the production of growth substances (Coombe, 1976; Hedden and Hoad, 1985). It is also possible to induce parthenocarpy by exogenously applied plant growth substances in many plants. For example, N-(2-chloro-4-pyridyl)-N’ –phenylurea (CPPU), a synthetic cytokinin, is effective on fruit set and development in some fruit crops and vegetable crops (Bangerth and Schroeder, 1994; Shudo, 1994; Lewis et al., 1996).
Cytokinins have been linked to virtually all stages of the cell cycle (D’Agostino and Kieber, 1999), which is usually divided into four phases: G1, S, G2, and M. Progression through the eukaryotic cell cycle is largely regulated at two principal control points, during the late G1 phase and at the G2/M boundary (Stals and Inzé, 2001). The late G1 restriction (R) point is particularly significant, since cells must interpret extracellular signals and either commit to a further round of division or adopt alternative differentiation pathways (Pardee, 1989). In animals, this process is mediated by D-type cyclins (Sherr, 1993). Recent studies showed that plant D cyclins exhibited expression patterns reminiscent of animal D-type cyclins, including rapid transcript accumulation upon stimulation of quiescent suspension-cultured cells with growth-promoting substances (Dahl et al., 1995; Soni et al., 1995; Fuerst et al., 1996). Furthermore, plant CycD cyclins share the presence of the retinoblastoma protein (Rb)-binding motif LxCxE with their mammalian homologues (Ach et al., 1997; Huntley et al., 1998). These results suggest that plant CycD cyclins may, like animal D-type cyclins, regulate G1 controls through interactions with plant Rb proteins (Gutiérrez, 1998; Sorrell et al., 1999). In addition to a role in the G2/M transition (Redig et al., 1997; Zhang et al., 1996; Hare and van Staden, 1997), cytokinins have been shown to increase cell proliferation, at least in part, via the induction of CycD3 at the G1-S cell cycle phase transition (Riou-Khamlichi et al., 1999).
Lagenaria leucantha is an important vegetable crop widely grown in greenhouses throughout Asia. It is a monoecious annual cucurbit plant, which can climb up to a height of 3 m. However, the plant grown in the greenhouse rarely fruits during the autumn and spring because the plant produces almost all female flowers with a few male flowers. In previous work, it has been shown that CPPU can effectively promote cell division and induce parthenocarpy in Lagenaria leucantha (Yu, 1999; Yu et al., 2001a). This not only provides an effective solution to the ovary abortion, but also provides an experimental system for studying fruit development, in particular, the mechanism of chemical-induced parthenocarpy. Owing to the significant role of CPPU in inducing parthenocarpy and promoting cell division, the question arose whether CPPU affects the expression of CycD3. Here, full-length cDNA clones for two CycD3 genes from Lagenaria leucantha have been isolated and characterized. Effects of pollination/fertilization and CPPU on the expression of the CycD3 genes in fruits of Lagenaria leucantha were also studied. The results demonstrated that CycD3 is actively involved in the regulation of fruit development, and both pollination and CPPU trigger fruit growth, partly, at least, by regulating the expression of CycD3 genes.
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Materials and methods |
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Plant material
Plants of Lagenaria leucantha Rusby, cv. Hangzhou long-gourd were grown in a greenhouse, as reported earlier (Yu, 1999). Experiments consisted of three treatments: (A), non-pollination; (B), pollination; (C) non-pollination with CPPU (50 mg l–1) treatment. Unpollinated ovaries were prepared by bagging the female flowers (petals) before anthesis. CPPU was first dissolved in ethanol at a concentration of 2000 mg l–1 in the presence of 0.2% Tween 80, and then diluted to 50 mg l–1 with water. The solution was sprayed onto ovaries of previously bagged female flowers at anthesis. Ovaries were sampled at designated times, frozen quickly in liquid nitrogen and stored at –70 °C before use.
Determination of cell number
From the flesh of a fruit, 5-mm-thick slices were cut, subsequently fixed in a mixture of 70% ethanol, formaldehyde, and acetic acid (90:5:5 by vol.) and embedded in paraffin. Nine-µm-thick transverse sections were prepared from slices using a microtome (YL-3, Shanghai Instrument Co.). The sections were mounted, stained with toluidine blue, scanned and photographed under a microscope (Olympus PM-ADS). Cell numbers were calculated as described (Takeno et al., 1992).
RNA extraction
Total RNA from fruits was extracted by grinding the fruit tissue in a mortar in the presence of TRIzol Reagent (GIBCO/BRL) according to the manufacturer’s instructions. After extraction, total RNA was dissolved in diethyl pyrocarbonate-treated water.
Reverse transcription of mRNA and PCR
A pair of degenerated primers (P1: 5'-TGGATGABTCARCTT GYTGCTG-3' and P2: 5'-GTCACYRGATKCATYYTCC-3') based on the conserved sequences of CyclinD3 (WMTQLAAV and WKMNPVT) was used for PCR amplification of Lagenaria leucantha CyclinD3 from both genomic DNA and cDNA. In the case of genomic DNA, a fragment of about 312 bp in length was amplified and named as LlCycD3;1. When cDNA was used as the template, the cDNA was first synthesized from total RNA of the young ovary using an anchored-(dT)15 primer (P3'-anchor: 5'-GGCCACGCG TGGTCAAC(T)15-3'). PCR was performed with P1 and P2 primers, and a fragment of about 182 bp was isolated (named as LlCycD3;2). Both fragments were cloned into a pGEM-T vector (Promega) and sequenced at the DNA Sequencing Facility, Biotechnology Institute, Zhejiang University. The DNA sequences were analysed by BLAST search, and revealed that the cloned sequences were part of CyclinD3 genes.
RACE cDNA cloning
To isolate full-length cDNA clones of LlCycD3;1 and LlCycD3;2, 3' and 5' rapid amplification of cDNA ends (RACE) was carried out (Frohman et al., 1988). For 3'-RACE, the first round of PCR was performed with P1 and P3'-RACE (5'-GGCCACGCGTGGTC AACT-3') primer pair using first-strand cDNA as template. The nested PCR was then performed with P3'-RACE and specific primer P3 (5-AGTGGAGGAGACCCAAGTTC-3') for LlCycD3;1 and P4 (5-AGTCGAAGAAATTCGT GTCC-3') for LlCycD3;2, designs based on the sequences obtained above, respectively.
In the 5'-RACE, primers specific for two CycD3 genes were designed according to the cDNA sequence of the 3' region determined by 3'-RACE: LlCycD3;1: P5: 5'-AGAGAGCACA AGAAGCTCCAT-3', P6: 5'-ATGGGGTAACAGGATTCAT-3'; LlCycD3;2: P7: 5'-GGACACGAATTTCTTCGACT-3', P8: 5'-AGTAAGCACTAAAA GCTCCAT-3'. In initial 5'-RACE experiments, the first strand cDNA prepared as above, was purified and dC tailed by Terminal Deoxynucleotidyl Transferase (MBI Fermentas) according to the manufacturer’s instructions. The product was amplified via PCR with the first specific primer (P6 for LlCycD3;1; and P8 for LlCycD3;2) and PG (oligo-(dG)16). The nested PCR was carried out with the second CycD3 specific primer (P5 for LlCycD3;1; and P7 for LlCycD3;2) and PG on the product of first PCR and the resulted PCR products were cloned into pGEM-T vector and sequenced.
Southern blot analysis
Genomic DNA was isolated from leaves of Lagenaria leucantha with minor modifications of the CTAB protocol (Doyle and Doyle, 1990). Ten micrograms of DNA was digested with restriction enzymes, HindIII, SpelI, EcoRV, and XhoI; subjected to electrophoresis in a 1% agarose gel, blotted onto nylon membranes (Hybond N+, Amersham Pharmacia Biotech) using standard procedures (Maniatis et al., 1989). The probes specific for LlCycD3;1 and LlCycD3;2 correspond, respectively, to the 867 bp and 939 bp fragments produced by 3'-RACE. The probes were labelled by 
-32P-dCTP (3000 Ci mmol l–1) with the Random Primed DNA Labelling Kit (Promega). Hybridizations were carried out overnight at 60 °C. Membranes were washed using standard procedures (Maniatis et al., 1989) and analysed by Typhoon 8600 (Pharmacia).
Northern blot analysis
RNA (10 µg) was separated in a denaturing 1.2% (w/v) agarose gel containing 2% formaldehyde and blotted onto a Hybond N+ membrane. Relative loading was confirmed by subsequent running of the samples and using UV fluorescence of the ethidium bromide stain. Probe preparation and visualization of hybridized bands were carried out according to standard procedures.
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Isolation of cDNAs for D3 cyclins
DNA fragments of 312 bp and 182 bp were amplified by degenerated PCR with genomic DNA and cDNA as the template, respectively (data not shown). The nucleotide sequences of the two fragments were used for the synthesis of primers in the 3'-RACE cloning (P3 for LlCycD3;1 and P4 for LlCycD3;2). The two 3'-cDNA clones produced were of 867 bp (for LlCycD3;1) and 939 bp (for LlCycD3;2) in length, respectively. The 5'-specific primers were designed and two different CycD3 full-length cDNA clones, LlCycD3;1 with 1648 bp and LlCycD3;2 with 1565 bp in length, were obtained. LlCycD3;1 and LlCycD3;2 contained open reading frames encoding putative proteins with 353 and 381 amino acids, respectively (Fig. 1).
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The predicted amino acid sequences of LlCycD3;1 revealed 38.5%, 47.3%, 49.0%, and 50.4% identities to the published D3 cyclins from Arabidopsis, Lycopersicon, Antirrhinum, and Medicago, while identities were 34.6%, 37.8%, 38.2%, and 38.1% for LlCycD3;2, respectively. Similar to other D-class cyclins, LlCycD3 contained a conserved cyclin box region of approximately 100 amino acids (amino acids 85–185 in LlCycD3;1 and 100–200 in LlCycD3;2, boxes in Fig. 1). In addition, the predicted proteins of LlCycD3 displayed two characteristic structural elements of D cyclins; the motif LxCxE in the N-terminus and possible PEST regions in the C-terminus of both cyclins (Fig. 1). In common with CycD3 sequences isolated so far from other plants, LlCycD3 displayed an acidic residue (D) at position 2 relative to the LxCxE motif. Using the PESTFIND software available on the European Molecular Biology Network (EMBnet) Austria server (http://www.at.embnet.org/embnet/tools/bio/PESTfind/), one potential PEST sequence was identified between positions 304 and 360 of LlCycD3;2 with a PEST score of +12.47, while for LlCycD3;1 it was +4.78, and between positions 290 and 330.
Phylogenetic analysis using the complete amino acid sequences of plant D3 cyclins by the multiple alignment program CLUSTAL W showed that LlCycD3 was very close to Lycopersicon esculentum D3;3 and Antirrhinum majus D3a (Fig. 2). Southern blot analysis showed that both LlCycD3;1 and LlCycD3;2 were present in a low copy number per genome (Fig. 3).
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Fruit growth and cell division
Unpollinated ovaries did not develop further and the cell number remains almost unchanged (Figs 4, 5). Pollinated- or CPPU-treated unpollinated ovaries grew to the normal size. Significantly, the growth of the CPPU-induced fruit was much faster than the pollinated fruit (Fig. 4). The cell number of pollinated fruit increased after anthesis and cell division occurred mainly in the first 4 DAA (day after anthesis). A similar trend was also observed with the CPPU treatment, except that the effect was greater compared with pollination (Fig. 5).
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Expression of CycD3 genes
Northern analysis showed that the CycD3;1 transcript was most abundant at anthesis. The transcript levels of CycD3;1 in the unpollinated ovaries sharply decreased after anthesis and could not be detected from 2 DAA.. The expression of LlCycD3;1 was stimulated either by pollination/fertilization or CPPU, and the effect of CPPU was more pronounced (Fig. 6). In accordance with changes in cell division, low transcript levels were observed in pollinated and CPPU-treated ovaries at 8 DAA and 12 DAA. Almost no transcript of CycD3;2 was observed in unpollinated ovaries. Following pollination, the transcript of CycD3;2 peaked at 4 DAA, and subsequently decreased gradually. CPPU treatment resulted in a higher CycD3;2 transcription level just after anthesis, but decrease at 4 DAA (Fig. 6).
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Discussion |
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The two cyclin genes isolated from fruit of Lagenaria leucantha contain the characteristics of plant cyclin D3, and were nominated: LlCycD3;1 and LlCycD3;2 according to the nomenclature rules of Renaudin et al. (1996). As far as is known, they represent the first CycD3 genes isolated from the Cucurbitaceae. Similar to other CycD3, the predicted amino acid sequences of LlCycD3 contained a Cyclin box, a LxCxE motif and possible PEST regions. The Cyclin box is postulated to encode a domain that interacts with Cyclin-Dependent Kinases (Jeffrey et al., 1995). The LxCxE motif binds to retinoblastoma-related proteins (Sherr, 1993; Renaudin et al., 1996). The PEST regions ensure that D3 cyclins can be rapidly turned over and proteolytically degraded (Rogers et al., 1986; Rechsteiner and Rogers, 1996). Southern blot analysis showed that there were two genes encoding D3 cyclins in Lagenaria leucantha, which is in accordance with the results from tomato and Arabidopsis (Soni et al., 1995; Kvarnheden et al., 2000; Vandepoele et al., 2002). These results further support the suggestion that there is a small family of D3 cyclin genes in dicotyledonous plants (Kvarnheden et al., 2000).
Generally, the two LlCycD3 genes showed different expression patterns during fruit development (Fig. 6). LlCycD3;1 showed the highest expression at anthesis whereas LlCycD3;2 showed higher expression levels at 2 DAA and 4 DAA in the CPPU-induced fruits and pollinated fruits, respectively. It seems likely that both LlCycD3;1 and LlCycD3;2 are developmentally regulated and they have different roles in the control of cell cycle progression. Different expression patterns have been detected for two D3 cyclins in Antirrhinum and tobacco (Doonan, 1998; Sorrell et al., 1999). Accordingly, the specific function for two D3 cyclins in Lagenaria leucantha remains to be further determined.
D-type cyclins are thought to link environmental and developmental cues to the cell cycle (Meijer and Murray, 2000). For example, plant cyclin D genes are regulated in response to exogenous signals known to affect the growth of plant cells. Cytokinins were shown to activate Arabidopsis cell division through the induction of CycD3 in whole plants, as well as in tissue culture (Riou-Khamlichi et al., 1999). Over-expression of D-type cyclins not only reduced the length of the G1 phase, but also partially overrode the need of dividing cells for mitogens (Kato and Sherr, 1993; Zwijssen et al., 1996). By contrast, CycD3 of alfalfa was not induced by cytokinins and the overproduction of CycD3 in alfalfa had no obvious effect (Jeleñska et al., 2000). As observed in previous studies (Yu et al., 2001a), cell division practically ceased after anthesis in unpollinated ovaries. Both pollination and CPPU treatment, however, were able to reactivate cell division, with CPPU being more effective. In accordance with the changes in cell number, CycD3 accumulated from pollination/fertilization or CPPU treatment onwards and the effect of CPPU was more rapid than pollination/fertilization. It is likely that CPPU and pollination played a similar role in activating CycD3 expression and they increased cell division by increasing CycD3 expression in fruits of Lagenaria leucantha. For example, CPPU treatment resulted in a high transcription level of CycD3;2 after anthesis and it reached the highest level at 2 DAA. In pollination, however, CycD3;2 transcripts peaked at 4 DAA after a very low level of transcription at 2 DAA (Fig. 6). The delay observed in pollinated ovaries could be explained by the time needed for fertilization. Endogenous cytokinin production was low during the first days after pollination, and the concentration of endogenous cytokinins such as zeatin in the ovary was lower than that in CPPU treatment tissues (Yu et al., 2001b). These results are consistent with a direct action of cytokinins on CycD3 expression and also supports that CPPU has intrinsic cytokinin properties and possibly the same mode of action as endogenous cytokinins (Karanov et al., 1992; Shudo, 1994). CPPU promoted the expression of CycD3 in parthenocarpic fruit growth and the regulation of expression of the CycD3 gene appears to be a key mechanism by which cytokinins influence cell proliferation and fruit development.
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Acknowledgements |
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This work has been supported by the National Natural Science Foundation of China, 863 plan, Excellent Teacher Foundation of China and Natural Science Foundation of Zhejiang Province as a special project. We also appreciated the help and suggestions of Professor Dirk Inzé (Department of Systems Biology, VIB, Belgium).
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