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First published online July 8, 2009; 10.1104/pp.109.135822 Plant Physiology 151:391-399 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Null Mutation of the MdACS3 Gene, Coding for a Ripening-Specific 1-Aminocyclopropane-1-Carboxylate Synthase, Leads to Long Shelf Life in Apple Fruit1,[W],[OA]Laboratory of Plant Breeding and Genetics, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki 036–8561, Japan (A.W., J.Y., H.K., A.K., T.H.); National Institute of Agrobiological Science, Tsukuba 305–8602, Japan (Y.W.); Aomori Prefectual Industrial Technology Research Center, Hirosaki 036–8363, Japan (Y.H., M.I.); and Laboratory of Fruit Cell and Molecular Breeding, College of Agronomy and Bio-tech, China Agricultural University, Beijing 100193, China (T.L.)
Expression of MdACS1, coding for 1-aminocyclopropane-1-carboxylate synthase (ACS), parallels the level of ethylene production in ripening apple (Malus domestica) fruit. Here we show that expression of another ripening-specific ACS gene (MdACS3) precedes the initiation of MdACS1 expression by approximately 3 weeks; MdACS3 expression then gradually decreases as MdACS1 expression increases. Because MdACS3 expression continues in ripening fruit treated with 1-methylcyclopropene, its transcription appears to be regulated by a negative feedback mechanism. Three genes in the MdACS3 family (a, b, and c) were isolated from a genomic library, but two of them (MdACS3b and MdACS3c) possess a 333-bp transposon-like insertion in their 5' flanking region that may prevent transcription of these genes during ripening. A single nucleotide polymorphism in the coding region of MdACS3a results in an amino acid substitution (glycine-289  valine) in the active site that inactivates the enzyme. Furthermore, another null allele of MdACS3a, Mdacs3a, showing no ability to be transcribed, was found by DNA sequencing. Apple cultivars homozygous or heterozygous for both null allelotypes showed no or very low expression of ripening-related genes and maintained fruit firmness. These results suggest that MdACS3a plays a crucial role in regulation of fruit ripening in apple, and is a possible determinant of ethylene production and shelf life in apple fruit.
The plant hormone ethylene plays an important role in the regulation of fruit ripening (Capitani et al., 1999  ). Many ripening processes are driven by ethylene-regulated changes in gene expression, especially in climacteric fruit exhibiting a high respiration rate during ripening, such as apple (Malus domestica) and tomato (Solanum lycopersicum; Giovannoni, 2001). The level of ethylene in plants is determined by the activity of the key enzyme 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS). In ripening apple fruit, ethylene production is strictly related to the level of MdACS1 expression (Sunako et al., 1999; Harada et al., 2000). Moreover, differential expression of MdACS1 allelic forms (MdACS1-1 and -2) among different cultivars causes differences in the extent of preharvest fruit drop, which is a physiological effect of the ethylene level in the fruit (Harada et al., 2000; Sato et al., 2004). However, the polygalacturonase gene (MdPG1), which is involved in softening of fruit flesh (shelf life), was transcribed differently in cultivars with the same MdACS1 allelic forms (Oraguzie et al., 2004), suggesting that other factor(s) are correlated with the trait of shelf life.
On the basis of the level of ethylene production during fruit development, McMurchie et al. (1972)
In pear (Pyrus communis) and Japanese pear (Pyrus pyrifolia), other ACS genes in addition to the gene homologous to MdACS1 have been reported to determine the ripening behaviors of various cultivars (Itai et al., 1999
Structure and Organization of MdACS3
Three positive phage clones were isolated from the genomic library of cv Golden Delicious by screening with a probe DNA from the last exon of MdACS3. The sequence of one of the three clones corresponded to that of MdACS3 (accession no. U73816; Rosenfield et al., 1996
Three MdACS3 Genes Located at Distinct Loci
To investigate the relationship among these MdACS3 genes, we performed cleaved-amplified polymorphic sequence (CAPS) analysis using HindIII and EcoRI sites (Fig. 1) that produce diverse fragments from the respective MdACS3 genes (Fig. 2
). The results indicated that the genomes of the six cultivars and 56 strains tested had all three MdACS3 genes. Then we performed linkage analysis of each MdACS3 gene using two F1 progenies (Igarashi et al., 2008
High Amount of Inserted Sequence in Malus, But Not in Pyrus
As shown in Figure 1, MdACS3b and MdACS3c possess extra sequence (333 bp) that is not present in MdACS3a. This sequence is flanked by the 8-bp terminal inverted repeat (5'-AATTTTTA-3') located at –570 of MdACS3a (accession no. AB243060). Querying this insertion in GenBank revealed that it is a miniature inverted-repeat transposable element (MITE; Bureau et al., 1996
MdACS3 Expression Precedes MdACS1 Expression Northern hybridization using different apple tissues (Fig. 4 ) revealed no transcription of MdACS3 in non-fruit organs, suggesting that its expression may be fruit specific. The cDNAs synthesized from total RNA of Golden Delicious on-tree fruit were analyzed by CAPS, in which the last exon of MdACS3a was amplified and double digested by HindIII/EcoRI and then electrophoresed on 2% agarose gel. The band pattern of the digested cDNA was the same as that from MdACS3a (Fig. 5 ), suggesting that only the transcript of MdACS3a is present in apple fruit.
To test the expression pattern of the MdACS3a gene during fruit ontogeny, we carried out northern hybridization of RNA fractions extracted from fruits that were sampled weekly from the full blossom to ripening stages (Supplemental Fig. S2). Expression of MdACS3a began before the commercial harvest day, but MdACS1 and MdACO1 were expressed only after commercial harvest. These results indicate that MdACS3a functions as a ripening-specific gene, like MdACS1 and MdACO1, at least 2 weeks before the burst of ethylene production caused by expression of MdACO1 and MdACS1. Figure 6 shows changes in ethylene production and expression of ripening-related genes, including MdACS3a, in Golden Delicious fruit. A strong signal of MdACS3a was observed on October 9, when MdACS1, MdACO1, and MdPG1 had not yet begun to be expressed, and persisted to October 27. Expression of MdACS3a decreased gradually from October 21 after the massive increase in MdACO1 and MdACS1 expression, suggesting that expression of MdACS3a is suppressed when fruit enter ripening with a burst of ethylene production. To investigate whether the expression of MdACS3a is affected by ethylene, we analyzed its transcript in 1-MCP-treated fruit (Golden Delicious). The expression of MdACS1, MdACO1, and MdPG1 was completely inhibited by 1-MCP treatment, but the signal of MdACS3a expression was observed until day 12 (Fig. 7 ).
A Null Mutation Exists in the Apple Genome
El-Sharkawy et al. (2004)
To test whether this amino acid substitution affects the enzyme activity of ACS3a, full-length cDNAs of ACS3a and ACS3a-G289V were constructed into the expression vector pET11d. As a positive control, cDNA of MdACS1 (Sunako et al., 1999
MdACS3a Allelic Genotypes Determined by the Genomic and cDNA Sequences The ACS3a allelic genotype of each cultivar was determined from the relative abundance of SNPs in genomic and cDNA sequences, which were analyzed by direct sequencing (Supplemental Fig. S3). Cultivars with either G alone or T alone in both their genomic and cDNA sequences were identified as ACS3a/ACS3a or ACS3a-G289V/ACS3a-G 289V, respectively (Supplemental Fig. S3, A or B). Cultivars having both G and T in their genomic and cDNA sequences were identified as ACS3a/ACS3a-G289V (Supplemental Fig. S3C). During the SNP analyses, some cultivars were assessed as ACS3a/ACS3a-G289V in their genomic sequence, but only ACS3a-G289V was found in the cDNA sequences. For example, in apple cv Kitaro, two peaks (G and T) appeared in the sequencing trace for genomic DNA but only one peak (T) appeared in the cDNA sequence (Supplemental Fig. S3D). This result suggests that a null gene, with no ability to be transcribed, exists in some apple varieties, and it was designated as Mdacs3a. Thus the allelic genotype of Kitaro is acs3a/ACS3a-G289V. Consequently, we were able to infer the genotype of apple cv Fuji from that of Kitaro, the progeny derived from a cross between cultivars Fuji and Hatsuaki (ACS3a-G289V/ACS3a-G289V), indicating that Fuji is ACS3a/acs3a. Supplemental Table S1 lists the ACS3a allelic genotypes of the apple cultivars we have investigated. Thus, we conclude that ACS3a is inactive in ACS3a-G289V/ACS3a-G289V and acs3a/ACS3a-G289V cultivars.
To develop a DNA marker to identify MdACS3a alleles, we analyzed the promoter region of each allele from several apple cultivars. The promoter region (–90 to –530) of each cultivar was cloned and sequenced. A dinucleotide GA repeat sequence (simple sequence repeat [SSR]) was found at –420 of the promoter, and contained 20 repeats in mutated ACS3a-G289V but only nine repeats in wild-type ACS3a (Fig. 9A ). Sequencing the counterpart region of ACS3a amplified from the wild species Malus coronaria (ACS3a-G289V/ACS3a-G289V) showed 20 repeats in the SSR, suggesting that the repeat polymorphism is linked to the respective SNPs of ACS3a and ACS3a-G289V.
The SSR region of each cultivar was amplified and run on 6% polyacrylamide gels (Fig. 9B). It is possible to identify from the band pattern whether apple cultivars contain the ACS3a-G289V allele. Supplemental Fig. S5 shows the presence of ACS3a-G289V allele in the apple cultivars and wild species we have investigated. ACS3a-G289V was found in the wild species M. coronaria, indicating that this mutation occurred before apple domestication. In addition, ACS3a-G289V exists not only in cultivars bred in Japan but also in those bred in other countries such as New Zealand, America, and Australia (Supplemental Fig. S5).
Figure 10
shows changes in ethylene production and expression of ripening-related genes in apple cultivars Kitaro and Kotaro that are derived from the same cross parents. Ethylene production was much higher in Kotaro than in Kitaro. Expression of MdACS1 was not detected in Kitaro by northern blotting, but distinct bands were observed in Kotaro after storage at 24°C for 3 to 9 d. Trace expression of MdACS3a was detected in Kitaro, whereas the expression was quite strong in Kotaro. Although MdACO1 was expressed in both cultivars, it was much stronger in Kotaro. Expressions of MdPG1, which is related to the softening of apple fruit (Wakasa et al., 2006
Levels of ethylene production in ripening fruit are broadly in agreement with the presence of particular MdACS1 allelic forms (Sunako et al., 1999 ; Harada et al., 2000). However, there are differences even within the same allelic forms, suggesting the effect of other ripening-related MdACS gene(s) (Rosenfield et al., 1996), as shown in pear fruit (Itai et al., 1999; El-Sharkawy et al., 2004). By screening a genome DNA library, we identified another ACC synthase gene subfamily in apple, MdACS3. Two of the genes in the subfamily, MdACS3b and c, are not transcribed to mRNA because of a transposon insertion, and thus only MdACS3a is functional. Furthermore, MdACS3a in some cultivars is present as a mutant allele, MdACS3a-G289V, in which a single nucleotide polymorphism leading to a single amino acid substitution results in an inactive protein. In addition, another allele, Mdacs3a, is found as a null allele because of failure of transcription. The existence of these three alleles made it possible to relate differences in ethylene production to shelf life among apple cultivars.
In apple, expression of MdACS3 preceded that of MdACS1 and MdACO1, and decreased after the robust expression of MdACS1 and MdACO1 and the burst of ethylene production (Fig. 6; Wang et al., 2009
According to the phylogenetic relationships of the Maloideae reported by Campbell et al. (1995)
ACC synthase belongs to the group of pyridoxal-5'-phosphate-dependent enzymes, and residue K283 is necessary for pyridoxal-5'-phosphate binding (Capitani et al., 1999 Ethylene production was much lower in the Kitaro than in Kotaro, and the expression of ripening-related genes was also greatly suppressed in Kitaro (Fig. 10). A similar result was found in the comparison of Gala and Koukou (Supplemental Fig. S6). These differences can be explained by the respective MdACS3a allelotypes of these cultivars, because Kitaro and Koukou are acs3a/ACS3a-G289V with inactive ACS3a, whereas Kotaro and Gala are ACS3a/ACS3a-G289V with active ACS3a. In Kitaro and Koukou (Supplemental Fig. S7), system-2 ethylene synthesis may not occur because acs3a/ACS3a-G289V cannot produce sufficient ethylene to initiate the transition to system-2 ethylene synthesis, and thus downstream genes, especially MdPG1, were not expressed in Kitaro and Koukou. This supports the hypothesis that ACS3a acts as a switch to initiate the transition from system-1 to system-2 ethylene synthesis, subsequently leading to a burst of ethylene production. Thus, ACS3a is likely to be the main enzyme that controls ethylene production and shelf life of apple fruit. This conclusion was also supported from the data of other cultivars (Supplemental Table S2). Alignment of MdACS3a orthologs of more than 100 plant species revealed that the G289V mutation is found only in Malus, including wild species and domesticated cultivars from America, Australia, Europe, New Zealand, and Japan (Supplemental Fig. S5). It was not found in pear, although this species is very closely related to apple. These results indicate that the G289V mutation arose after separation of Malus from the Maloideae and was then maintained during domestication and inherited stably among the domesticated cultivars.
The difference between MdACS3a and the null gene Mdacs3a is still unclear, and understanding the difference will lead to development of a molecular marker for Mdacs3a. No transposon or other insertion was found in the promoter region of the null gene, suggesting that the difference might occur much further upstream of the promoter than we have investigated. Matarasso et al. (2005)
This study describes molecular evidence that accounts for the difference of apple fruit shelf life among cultivars. Out of three genes of ripening-specific MdACS3 family, only one (MdACS3a) expresses at the transition from system 1 to system 2 ethylene biosynthesis. We demonstrated here that the existence of three alleles of MdACS3a made it possible to relate differences in ethylene production to shelf life among apple cultivars. These results have allowed us to propose that MdACS3a plays a crucial role in regulation of fruit ripening in apple, and may be the main determinant of ethylene production and shelf life in apple fruit.
Plant Materials
Young expanding leaves of apple (Malus domestica) cultivars and wild species sampled from the experimental farms of Aomori Apple Experimental Station (Japan) and Hirosaki University were used as a source of genomic DNA, which was extracted as described by Sunako et al. (1999)
A genomic DNA library obtained from Golden Delicious (Sunako et al., 1999
Intact fruits were enclosed in a gas-tight container (0.8 L) equipped with septa and kept at 24°C for 1 h, then 1 mL of gas was sampled through the headspace of the container by a syringe. The ethylene concentration in the sample was measured with a gas chromatograph (Shimadzu) equipped with a flame ionization detector. Five fruits per sample were measured.
Flesh firmness was measured with a hand-held penetrometer (FT-327; Facchini) fitted with an 11-mm-diameter probe. Four skin discs (approximately 2.5 cm in diameter) were removed from opposite sides of each fruit. The probe was pressed into the tissue of the cut surface to a depth of 8 to 9 mm in a single smooth motion. Five fruits per sample were measured.
Golden Delicious fruits were treated with 1 µL L–1 of 1-MCP (EthylBloc; Rohm and Haas) for 15 h at 24°C. After treatment, fruits were held at 24°C and sampled every 3 d.
Genomic DNA extraction and Southern-blot analysis were performed as described by Sunako et al. (1999)
RNA extraction and northern gel-blot analysis were performed as described by Sunako et al. (1999)
MdACS3 genes in the genome of apple cultivars were amplified by PCR, which was performed with primers ACS3-17 and ACS3-8 for the first PCR, and ACS3-7 and ACS3-14 (Supplemental Table S3) for the second PCR. The product digested with EcoRI and HindIII was electrophoresed on a 2% agarose gel. Two micrograms of total RNA extracted from the fruit was used for first-strand cDNA synthesis (Superscript II RT, Invitrogen) with primer ACS3-8, and the subsequent PCR was carried out with the same primers as for amplification of genomic DNA.
cDNAs for MdACS3a and MdACS3a-G289V were amplified by PCR with ACS3a cDNA as template and the primers ACS3a infu-1 and ACS3a infu-2 (Supplemental Table S3). cDNA for MdACS1 (accession no.U89156) was amplified with the primers ACS1 infu-1 and ACS1 infu-2 (Supplemental Table S3). The PCR products were then ligated to the NcoI/BamHI double-digested 5.7 kb pET1ld (Stratagene) vector by using In-Fusion Dry-Down PCR cloning kit (CLONTECH) according to the manufacturer's instructions. Those recombinants containing the correct sequence were identified and retransformed into an Escherichia coli host, BL21 (DE3; Novagen). BL21 (DE3) cells harboring a pET11d-ACS3 and pET11d-ACS1 recombinant plasmid were grown on an Luria-Bertani (LB) plate in the presence of 100 µg/mL ampicillin. LB medium (5 mL) containing 100 mg/mL ampicillin was inoculated with a single colony and incubated at 37°C overnight with constant shaking. The overnight culture (5 mL) was transferred into 500 mL of LB medium. Cells were grown at 30°C with constant shaking. When the cell density reached OD600 of 0.5, isopropyl-β-D-thiogalactopyronoside was added to the cell culture to a concentration of 0.1 mM. The culture was then transferred to room temperature (20°C–25°C) for 5 more hours with constant shaking. The cells were harvested by centrifugation at 4,000g for 10 min at 4°C. Cell pellets were stored at –70°C for later use.
Protein concentration was quantified using the Bio-Rad protein assay with bovine serum albumin as a standard. Two-dimensional electrophoresis was performed with the ReadyPrep 2-D starter kit (Bio-Rad) according to the instruction manual. Briefly, immobilized pH gradient strips (7 cm, pH 3–10; Bio-Rad ReadyStrip, Bio-Rad) were rehydrated overnight with 125 µL of sample buffer containing 87.5 µg of total protein. Proteins were focused in a PROTEAN IEF cell (Bio-Rad) at 20°C for 12 h, applying 250 V (15 min), 4,000 V (120 min), and 4,000 V for a total of 20 KVh. After isoelectric focusing, strips were equilibrated in equilibration buffers I and II for 10 min, respectively. Two-dimensional SDS-PAGE was run in acrylamide gels (Ready Gel precast gel, Bio-Rad) at 200 V for 45 min. Gels were stained with colloidal CBB G-250.
ACC synthase extract was prepared according to the method of Li et al. (1996)
For sequence analysis of genomic DNA of MdACS3a to determine the genotype, a first PCR was performed with primers MdACS3a-1F and MdACS3a-2R (Supplemental Table S3) and genomic DNA as template. For SNP sequencing, a second PCR was conducted with the primers MdACS3a-2F and MdACS3a-2R with the first PCR product as the template. All cycle sequencing reactions for DNA sequence analysis were performed using Big Dye terminator chemistry (Applied Biosystems) according to the manufacturer's protocols, and sequences were determined using an ABI 310 automated DNA sequencer.
For SSR analysis, primers MdACS3a-1F and MdACS3a-1R were used to amplify the SSR region from the first PCR product. PCR product was run on 6% polyacrylamide gel and stained with silver according to Bassam et al. (1991) Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers AB243060, AB243061, and AB243062.
The following materials are available in the online version of this article.
We thank the Aomori Apple Experimental Station for providing the plant materials used in this study. Received January 16, 2009; accepted June 28, 2009; published July 8, 2009.
1 This work was supported by the Program for Promotion of Basic Research Activities for Innovative Bioscience (PROBRAIN) in Japan. 
2 These authors contributed equally to the article. 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: Takeo Harada (tharada{at}cc.hirosaki-u.ac.jp).
[W] The online version of this article contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.135822 * Corresponding author; e-mail tharada{at}cc.hirosaki-u.ac.jp.
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