JXB Advance Access originally published online on March 10, 2006
Journal of Experimental Botany 2006 57(6):1281-1289; doi:10.1093/jxb/erj097
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RESEARCH PAPER |
The involvement of 1-aminocyclopropane-1-carboxylic acid synthase isogene, Pp-ACS1, in peach fruit softening
National Institute of Fruit Tree Science, NARO, Fujimoto, 2-1 Tsukuba, Ibaraki 305-8605, Japan
* To whom correspondence should be addressed. E-mail: tatsuki{at}affrc.go.jp
Received 6 October 2005; Accepted 13 December 2005
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Abstract |
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Ethylene promotes fruit ripening, including softening. The fruit of melting-flesh peach (Prunus persica (L). Batsch) cultivar ‘Akatsuki’ produces increasing levels of ethylene, and the flesh firmness softens rapidly during the ripening stage. On the other hand, the fruit of stony hard peach cultivars ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ does not soften and produces little ethylene during fruit ripening and storage. To clarify the mechanism of suppression of ethylene production in stony hard peaches, the expression patterns of four ethylene biosynthesis enzymes were examined: ACC synthases (Pp-ACS1, Pp-ACS2, and Pp-ACS3) and ACC oxidase (Pp-ACO1). In the melting-flesh cultivar ‘Akatsuki’, Pp-ACS1 mRNA was dramatically induced after harvesting, and a large amount of ethylene was produced. On the other hand, in stony hard peaches, Pp-ACS1 mRNA was not induced during the ripening stage, and ethylene production was inhibited. Since Pp-ACS1 mRNA was induced normally in senescing flowers, wounded leaves, and wounded immature fruit of ‘Yumyeong’, Pp-ACS1 was suppressed only at the ripening stage, and was not a defect in Pp-ACS1. These results indicate that the suppression of fruit softening in stony hard peach cultivars was caused by a low level of ethylene production, which depends on the suppressed expression of Pp-ACS1.
Key words: ACC synthase, ethylene, softening, stony hard peach
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The plant hormone ethylene plays an important role in many developmental processes, such as seed germination, fruit ripening, and the senescence of various organs, and also mediates responses to many environmental stimuli such as touch, wounding, pathogen attack, and flooding (for a review, see Abeles et al., 1992
). Ethylene is biosynthesized from S-adenosyl-L-methionine (SAM) via 1-aminocyclopropane-1-carboxylic acid (ACC) (Adams and Yang, 1979). The first step is catalysed by ACC synthase and the second by ACC oxidase. ACC synthase is generally the rate-limiting enzyme in the biosynthetic pathway. ACC synthase and ACC oxidase are encoded as multigene families, and their expressions are regulated by developmental and environmental factors (for reviews, see Kende, 1993; Zarembinski and Theologis, 1994).
In climacteric fruit, increases in ethylene production during fruit ripening correlate with a burst of respiration. Studies on transgenic tomato fruit in which ethylene production was suppressed (Hamilton et al., 1990; Oeller et al., 1991; Picton et al., 1993) or ethylene sensing was inhibited (Wilkinson et al., 1997) showed delayed fruit ripening and revealed a critical role of ethylene in fruit ripening.
Peach (Prunus persica (L). Batsch), a climacteric fruit, undergoes textural changes that lead to loss of tissue firmness during ripening that is accompanied by an increase in ethylene evolution. In melting-flesh peach, rapid softening occurs after harvest, resulting in a short shelf-life. In non-melting-flesh peach, softening is slow, and a dramatic reduction of flesh firmness does not occur even when the fruit is overripe. The differences in softening between melting-flesh and non-melting-flesh cultivars are attributed to the presence of endo-polygalacturonase (PG) activity during ripening (Pressey and Avants, 1973, 1978); melting-flesh peach has both endo- and exo-PG activity, whereas non-melting-flesh has only exo-PG activity.
Stony hard peaches barely soften on the tree or after harvest, although the fruit changes colour normally, contains highly soluble solids, and has good flavour (Haji et al., 2001, 2004). Genetic analysis indicated that stony hard (hd) is a recessive locus (Yoshida, 1976) and is different from the melting (M)/non-melting (m) locus (Haji et al., 2005). It has been assumed that a low level of ethylene production by stony hard peach is responsible for the inhibition of fruit softening, because exogenous ethylene softens them effectively (Haji et al., 2003; Hayama et al., 2003). Since ethylene production occurs and the fruit softens by the application of ACC, a precursor of ethylene, ACC oxidase activity and ethylene sensing are normal in stony hard peach (Haji et al., 2003). For this reason, it has been considered that ACC synthesis is the key in the stony hard peach fruit.
To date, one ACC synthase clone (Pp-ACS1; Mathooko et al., 2001) and two ACC oxidase clones (Pp-ACO1 and Pp-ACO2; Callahan et al., 1992; Mathooko et al., 2001; Ruperti et al., 2001) have been isolated from peach. The amount of Pp-ACO1 transcript increased strongly during ripening and in wounded tissues (leaves and preclimacteric fruit) (Callahan et al., 1992; Lester et al., 1994; Tonutti et al., 1997; Mathooko et al., 2001), but Pp-ACO2 mRNA was detected in fruit only during early development (Mathooko et al., 2001; Ruperti et al., 2001). Pp-ACS1 mRNA was induced during fruit ripening and by wound stimuli (Mathooko et al., 2001).
In this study, ethylene production and the expression patterns of three ACC synthase genes (Pp-ACS1, Pp-ACS2, and Pp-ACS3) and one ACC oxidase gene (Pp-ACO1) were examined in the stony hard peach cultivars ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ and the melting-flesh cultivar ‘Akatsuki’. It is reported here that Pp-ACS1 was suppressed during fruit ripening in stony hard peaches.
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Materials and methods |
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Plant materials and treatment
Plants of Prunus persica (L.) Batsch cv. ‘Akatsuki’ and cv. ‘Yumyeong’ were grown at the National Institute of Fruit Tree Science. Fruits of ‘Odoroki’ and ‘Manami’ were obtained from Nagano Prefecture. Flowers were collected immediately after the bloom and senescence stages. For wound treatment, leaves were collected from several sites in June and crushed with a haemostat. Fruit of ‘Akatsuki’ was harvested at commercial maturity and stored in the air at 25 °C. For propylene treatment of ‘Yumyeong’, ‘Odoroki’, and ‘Manami’, fruits were harvested at commercial maturity and placed in 78 l containers, and ventilated with a continuous flow of air or air containing 5000 µl l–1 propylene. These fruits were stored for the indicated times at 25 °C. For wound treatment, fruits were harvested at the seed-filling and pit-hardening stages, the preclimacteric stage (flesh firmness was 49–54 N 10 d before commercial maturity), and at commercial maturity (flesh firmness was 38–47 N). They were sliced into blocks (3 cmx0.5 cmx0.2 cm) and incubated at 25 °C. All samples were frozen in liquid nitrogen, and stored at –80 °C until use. Young leaves were collected at May for genomic DNA isolation.
Measurement of ethylene production and determination of flesh firmness
Flowers were placed in 75 ml glass vials. Wounded leaves were placed in 12 ml glass vials. Wounded fruits were placed in 12 ml glass vials. Harvested fruits were placed in an air-tight chamber. One ml of headspace gas was withdrawn from the glass vial or chamber for each measurement and injected into a gas chromatograph (model GC-14B, Shimadzu, Kyoto, Japan) equipped with an activated alumina column and flame ionization detectors. After removal of a small disc of skin from each side of the fruit, flesh firmness was measured with a penetrometer (Italtest, FT011, 8 mm diameter).
RNA extraction and isolation of cDNA
Total RNAs of whole flowers and leaves were extracted by the phenol–SDS method (Ausubel et al., 1987). Total RNA of fruits was extracted by the cetyltrimethylammonium bromide method followed by the phenol–SDS method (Tatsuki and Mori, 1999). First-strand cDNA was synthesized by reverse transcription from 5 µg of the total RNA from ‘Akatsuki’ flowers, leaves, and fruit. To screen for ACC synthase cDNAs, a PCR primer set was synthesized based on the conserved region of the nucleotide sequences of ACC synthase (Kende, 1993) [sense, 5'-CAAATGGGT(C/T)T(A/C/G/T)GC(T/A)GA(A/G)AATCAGCT-3'; antisense, 5'-CAT(A/G)TT(T/G)GC(A/G)AA(A/G)CAAAT(A/T)CG(A/G)AACCA(C/A)CCTGG(C/T)TC-3'].
Northern blot analysis
Five micrograms of total RNA was separated in a 1.0% agarose gel that contained 0.66 M formaldehyde, and was blotted onto a nylon membrane (Hybond N+, Amersham Biosciences). PCR fragments amplified with the following specific primer sets were used as probes: Pp-ACS1: sense, 5'-GTATAGCTTGCTTGCAAACCTCAC-3', antisense, 5'-GTATTCTCTCATTTAAACTGACCAC-3'; Pp-ACS2: sense, 5'-AAGAACCCAGAAGCCTCCAT-3', antisense, 5'-CAGGGCAATGGAAAGAAGAA-3'; Pp-ACS3: sense, 5'-GGGACAAATCAGAGGAGGAA-3', antisense, 5'-CAGAGCAGTGGCAAGAAGAG-3'; Pp-ACO1: sense, 5'-AGATGGAGAACTTCCCAATC-3', antisense, 5'-CAGGAATAGCAAACTAACAA-3'. The probes were labelled with PCR DIG Labeling Mix (Roche Diagnostics, Mannheim, Germany). Hybridization was performed in 7% SDS, 50% formamide, 5x SSC, 0.1% N-lauroylsarcosine, 2% blocking buffer (Roche Diagnostics), and 50 mM sodium phosphate (pH 7.0) at 55 °C. Membranes were washed twice for 15 min with 0.1x SSC, 0.1% SDS at 65 °C, and then exposed to X-ray film (Fuji Film, Tokyo, Japan).
Southern blot analysis
Genomic DNA was isolated from young leaves according to Dellaporta et al. (1983). Genomic DNA (5 µg) was digested with EcoRI, EcoRV, HindIII, SacI, and XbaI. Blotting and hybridization buffers were as for northern blot analysis. Hybridization was performed at 50 °C. Membranes were washed twice for 30 min with 0.5x SSC, 0.1% SDS at 65 °C.
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Results |
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In the fruit of ‘Akatsuki’, a melting-flesh peach, an increase in ethylene production and a decrease in flesh firmness began within 1 d after harvest (Fig. 1A, C). By contrast, the flesh of the stony hard peaches ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ remained hard, and ethylene evolution did not increase during storage (Fig. 1B, D). The application of propylene promoted softening of ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ fruits (Fig. 1D), and slight ethylene production occurred 3 d after treatment (Fig. 1B).
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To analyse the regulation of ethylene biosynthesis in stony hard peaches at the molecular level, cDNAs of the ethylene biosynthesis enzymes ACC synthase and ACC oxidase were isolated from peach. Two ACC synthase cDNA fragments were obtained from fruit and leaves by RT-PCR using degenerate primers. The nucleotide sequence of one cDNA clone was identical to that of Pp-ACS1 (accession no. AB044662). The other cDNA was identical to accession no. AF239987, reported previously, and was designated Pp-ACS2. The nucleotide sequence of two other ACC synthase isogenes were reported in the DDBJ data bank (accession nos AF239663 and AF239989). To isolate these cDNA fragments, RT-PCR was performed with specific primers on samples from flowers, leaves, and fruits. The ACC synthase clone with the same nucleotide sequence as AF239663 [GenBank] was isolated and designated Pp-ACS3. The cDNA clone of accession no. AF239989 was not amplified by RT-PCR using the two sets of specific primers.
The cDNA clones of Pp-ACS1 and Pp-ACO1 (accession no. AB044711), which included ORFs, were isolated from mature fruit by RT-PCR using sets of specific primers based on previous reports (Mathooko et al., 2001). These four clones (Pp-ACS1, Pp-ACS2, Pp-ACS3, and Pp-ACO1) were used as probes for northern blot analyses. Southern blot analysis showed that the cDNA probes of Pp-ACS1, Pp-ACS2, and Pp-ACS3 did not hybridize with each other (data not shown).
Figure 2 shows the expression patterns of ACC synthase and ACC oxidase genes in the fruits of Fig. 1. In ‘Akatsuki’, Pp-ACS1 mRNA was detected 1 d after harvest and Pp-ACO1 mRNA was expressed before a dramatic increase in ethylene evolution, then both transcripts became abundant. Expression of Pp-ACS2 and Pp-ACS3 could not be detected in fruit of either cultivar (data not shown). No expression of ACC synthase isogenes could be detected in ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ during fruit storage in air, but Pp-ACS1 mRNA was slightly detected 3 d and 5 d after propylene treatment in ‘Odoroki’ and ‘Yumyeong’. On the other hand, Pp-ACO1 mRNA was expressed at a constant level in stony hard peaches and was increased by propylene treatment. These results indicate that ethylene evolution did not occur after harvest in stony hard peaches because of a lack of expression of Pp-ACS1 in the fruit.
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To determine the ethylene production and expression patterns of ACC synthase and ACC oxidase genes in other organs, senescent flowers and wounded leaves and fruit were tested, in which large amounts of ethylene are biosynthesized generally (for a review, see Abeles et al., 1992
). ‘Yumyeong’ was used as the stony hard peach in further experiments. Ethylene was evolved more in the senescent flowers of both cultivars (‘Akatsuki’, 1.182±0.186 nl g–1 FW h–1; ‘Yumyeong’, 1.406±0.275 nl g–1 FW h–1) than in the flowers immediately after bloom (0.203±0.060, 0.515±0.085 nl g–1 FW h–1, respectively). Pp-ACS1 and Pp-ACO1 mRNAs accumulated in senescent flowers of both cultivars (Fig. 3). The expressions of Pp-ACS2 and Pp-ACS3 (data not shown) were not detected.
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Figure 4 shows the rate of ethylene production and the expression patterns of ACC synthase and ACC oxidase genes in wounded leaves. In both cultivars, ethylene production increased rapidly after wounding. The level of Pp-ACS2 mRNA increased rapidly within 0.5 h and then decreased. One h after wound treatment, the amount of Pp-ACS1 mRNA increased, and reached the maximum level 2 h after treatment. Pp-ACO1 mRNA was detected in intact leaves, and the amount of transcript increased after wounding. The expression of Pp-ACS3 was not detected (data not shown).
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The effects of wounding on the rate of ethylene production and on the expression patterns of ACC synthase and ACC oxidase in immature fruits were examined next. Ethylene production and the levels of all mRNAs increased after wounding in both cultivars (Fig. 5A, B). The maximum level of ethylene production and the maximum amounts of Pp-ACS1 and Pp-ACS2 mRNAs were higher in ‘Yumyeong’ than in ‘Akatsuki’ (Fig. 5A, B). The level of Pp-ACO1 mRNAs was very low in intact immature fruits of both cultivars, and was increased by wounding. In preclimacteric fruits, picked 10 d before commercial harvest, ethylene production was enhanced by wounding, reached the maximum level after 4 h, and then decreased in both cultivars (Fig. 6A). In ‘Akatsuki’, a second rise in ethylene evolution occurred after 24 h. The expression levels of Pp-ACS1 and Pp-ACS2 mRNAs were the same in both cultivars, and followed the patterns of ethylene production. The expression of Pp-ACS3 was not detected in these experiments (data not shown).
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In ripening fruit, wound-inducible ethylene production and expression patterns of ACC synthase and ACC oxidase mRNAs showed markedly different patterns between cultivars (Fig. 7). The fruit of ‘Akatsuki’ produced more ethylene, and levels were much greater than those in immature and pre-climacteric fruits (Figs. 5A, 6A, 7A). Pp-ACS1 mRNA was induced by wounding in both cultivars, but its level was higher in ‘Akatsuki’ (Fig. 7B). Pp-ACS2 was not expressed in ‘Akatsuki’ fruit, and was only slightly expressed in ‘Yumyeong’ fruit. The level of Pp-ACO1 mRNA was increased by wounding in ‘Akatsuki’, but it remained constant in ‘Yumyeong’ fruit. Pp-ACS3 was not detected in this experiment (data not shown).
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Figure 8 shows the DNA gel blot analysis of Pp-ACS1 in both cultivars. There were no marked differences in polymorphism between them.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Haji et al. (2001)
reported that the stony hard characteristic of peach was due to the absence of ethylene evolution during ripening. Since the fruit of the stony hard cultivar ‘Yumyeong’ can produce ethylene when ACC is applied, the lack of ripening-related ACC synthase activity has been considered to be the reason (Haji et al., 2003). In peach, only one ACC synthase isogene, Pp-ACS1, had been isolated, and analysis of its expression pattern showed that it was induced during ripening (Mathooko et al., 2001). Although Pp-ACS2 and Pp-ACS3 were isolated, northern blot analysis did not detect the transcripts in intact ripening fruit (data not shown). Since other ACC synthase genes could not be isolated in intact ripening fruit by RT-PCR, it was considered that Pp-ACS1 is the main ACC synthase gene that acts during fruit ripening. These findings indicate that, during ripening, expression of Pp-ACS1 mRNA was suppressed in stony hard peaches, resulting in the low level of ethylene production and the inhibition of fruit softening. It is assumed that the stony hard locus is related to the regulation of expression of Pp-ACS1 mRNA in ripening fruit.
Ethylene production dramatically increases not only during fruit ripening, but also in plants subject to stress, such as wounding, and in senescent tissues. Mathooko et al. (2001) reported that Pp-ACS1 was induced not only in ripening fruit, but also in wounded tissues. In this study, in senescing flowers and wounded immature and preclimacteric fruits of ‘Yumyeong’, ethylene production increased and transcripts of Pp-ACS1 were induced in those tissues (Figs 3–6
). These results indicate that in ‘Yumyeong’, Pp-ACS1 mRNA was normally expressed except in ripening fruit.
One possible mechanism of repression of Pp-ACS1 mRNA is the interruption of the ripening-related transcriptional activity by some insertion or deletion in the 5'-flanking region of Pp-ACS1, which contains a cis regulatory domain of ripening-related sequences. Sunako et al. (1999) reported that a short DNA element was inserted into the promoter region of apple ACC synthase, Md-ACS1, whose gene product was not detected during ripening. Since DNA gel blot analysis of Pp-ACS1 showed no marked differences in polymorphism in ‘Akatsuki’ and ‘Yumyeong’ (Fig. 8), it was assumed that there might be no insertion or deletion in the regulatory domain of Pp-ACS1 in ‘Yumyeong’. Another possible reason is disruption of a transcriptional factor that is specifically activated to induce Pp-ACS1 mRNA during fruit ripening. Furthermore, in ripening fruit of ‘Yumyeong’, some inhibitors might suppress the expression of Pp-ACS1. In ripening fruit of ‘Yumyeong’, the level of Pp-ACS1 mRNA was slightly lower than in wounded immature and mature fruits (Figs 5–7). By contrast, in ‘Akatsuki’, more abundant Pp-ACS1 mRNAs were induced by wounding as maturity advanced. To date, the mechanism that regulates Pp-ACS1 in stony hard peach is not clear, but a more comprehensive approach, such as a subtraction method using stony hard and non-stony hard peaches, will help to reveal it.
The process of fruit softening is complex and involves cell-wall degradation, which is regulated by many cell-wall-modifying enzymes (for reviews, see Brownleader et al., 1999; Brummel and Harpster, 2001). Comprehensive analysis of these enzymes during peach fruit ripening indicates that the softening begins before the climacteric rise, and genes whose expression starts before the climacteric rise are mostly down-regulated by ethylene, while genes with a ripening-specific expression are mostly up-regulated by ethylene (Trainotti et al., 2003). Since the flesh firmness of ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ fruit was reduced to about 40, 37, and 32 N in air (Fig. 1D), some cell-wall enzymes which are expressed in the absence of, or under a low level of, ethylene might activate in stony hard fruit. In stony hard peaches, lack of large amounts of ethylene production during late ripening might suppress the cell-wall enzymes that would otherwise be up-regulated by ethylene. These findings support the view of the role of ethylene in fruit softening.
Fruit ripening was delayed in transgenic tomatoes in which the biosynthesis of ethylene was suppressed (Hamilton et al., 1990; Oeller et al., 1991; Picton et al., 1993) or ethylene signal transduction was inhibited (Wilkinson et al., 1997). These results indicate that ethylene regulates various ripening processes, such as changes in colour and texture. However, in peach it seems that ethylene does not have an important role in fruit ripening without softening, because stony hard peach changes colour normally, contains highly soluble solids and produces good flavour. However, it is assumed that the concentration of ethylene might, nevertheless, be important in peach ripening because the little ethylene that stony hard peach produces might be sufficient for ripening without softening. The induction of late softening might require abundant ethylene.
Although ACC synthase is encoded by a multigene family, only three isogenes could be isolated. The copy number of genes in peach might be low because the genome size of peach is smaller than that of other fruit trees (peach, 262–265 Mbp; apple, 743–796 Mbp; pears, 496–536 Mbp in the haploid genome, Arumuganathan and Earle, 1991). The Pp-ACS3 cDNA fragment was amplified by RT-PCR, but no bands were detected by northern blot analysis in these experiments. Thus, the level of Pp-ACS3 cDNA expression is considered to be very low.
Pp-ACS1 was induced by wound stress (Mathooko et al., 2001). In this study, it is shown that the other peach ACC synthase gene, Pp-ACS2, was also induced by wounding. The expression pattern of Pp-ACS2 was slightly different from that of Pp-ACS1. The Pp-ACS2 mRNA was induced rapidly by wounding and reached the maximum level within 1 h, and then decreased, although the Pp-ACS1 mRNA remained for a prolonged period (Figs 4–6). Furthermore, Pp-ACS2 seemed to be negatively regulated by ethylene, because Pp-ACS2 mRNA was not induced in wounded ripening fruit, which produced abundant ethylene (Fig. 7). These results indicate that the two peach ACC synthase genes were differentially regulated in response to wounding (Figs 4–7). These biphasic expression patterns of ACC synthase isogenes has previously been reported in response to stresses such as wounding in potato and tomato (Schlagnhaufer et al., 1997; Tatsuki and Mori, 1999; Moeder et al., 2002).
Pp-ACO1 also has an important role in ethylene production during peach fruit ripening (Callahan et al., 1992; Lester et al., 1994; Tonutti et al., 1997; Mathooko et al., 2001). In ripening ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ fruits, constant levels of Pp-ACO1 mRNA were detected, but application of propylene to ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ fruits increased the levels of Pp-ACO1 transcripts (Fig. 2). Pp-ACO1 is up-regulated by ethylene (Tonutti et al., 1997; Ruperti et al., 2001), as are other ACC oxidase genes (Ross et al., 1992; Kim and Yang, 1994; Lassèrre et al., 1996; Lelièvre et al., 1997).
In conclusion, the stony hard peach cultivars ‘Yumyeong’, ‘Odoroki’, and ‘Manami’ produced little ethylene during fruit ripening, as a result of the inhibition of induction of Pp-ACS1 mRNA. These results indicate that Pp-ACS1 has an important role in the softening of peach fruit.
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Acknowledgements |
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We thank Dr H Mori, Dr H Ohkawa, and H Hayama for their valuable discussions. This work was supported in part by the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Grant-in-Aid for Young Scientists no. 15780031 to MT).
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Footnotes |
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Abbreviations: ACC, 1-aminocyclopropane-1-carboxylic acid; ACO, ACC oxidase; ACS, ACC synthase; PG, polygalacturonase; RT-PCR, reverse transcription-PCR.
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References |
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