Abstract
To evaluate gene expressions mostly engaged in early development of apple fruit, we performed the identification of transcripts differentially expressed in young fruit by using microarrays spotted with 6,253 cDNAs collected from young and mature apple fruits of the cultivar Fuji (Malus domestica Borkh. cv. Fuji). A total of 3,484 cDNAs out of 6,253 were selected after quality control of microarray spots and analyzed for differential gene expression patterns between young fruit and other tissues (mature fruit, leaf and flower). Among them, 192 cDNAs displayed a signal value higher than twofold in young fruit compared with other tissues. Blast analysis of the 192 cDNA clones identified 88 non-redundant groups encoding proteins with known function and 50 non-redundant groups with unknown function. The putative protein products were classified into the following categories: photosynthesis (16.7%), protein synthesis (12.3%), cell proliferation and differentiation (10.9%), cell enlargement (5.8%), metabolism (8.0%), stress response (7.2%), others (2.9%), and unknown functions (32.2%). Furthermore, confirming the microarray data by reverse transcription-polymerase chain reaction revealed that the wide range of transcripts differentially expressed in young fruit was expressed in other organs but not in the mature fruit. The data presented suggested that apple fruit development depends on the tight regulation of the expression of a number of genes, which are also expressed in other organs.
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Aharoni A, O’Connell AP (2002) Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. J Exp Bot 53:2073–2087
Arend M, Stinzing A, Wind C, Langer K, Latz A, Ache P, Fromm J, Hedrich R (2005) Polar-localised poplar K+ channel capable of controlling electrical properties of wood-forming cells. Planta 223:140–148
Biale JB (1964) Growth, maturation and senescence in fruits. Science 146:880–888
Callis J, Raasch JA, Vierstra RD (1990) Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. J Biol Chem 265:12486–12493
Campalans A, Pages M, Messeguer R (2001) Identification of differentially expressed genes by the cDNA-AFLP technique during dehydration of almond (Prunus amygdalus). Tree Physiol 21:633–643
Cuzin M (2001) DNA chips: a new tool for genetic analysis and diagnostics. Trnasfus Clin Biol 8:291–296
Dennis FG (1986) Apple. In: Moselise SP (ed) Handbook of fruit set and development. CRC, Boca Raton, pp 1–44
Dong Y-H, Janssen B-J, Bieleski LRF, Atkinson RG, Morris BAM, Gardner RC (1997) Isolating and characterizing genes differentially expressed early in apple fruit development. J Am Soc Hort Sci 122:752–757
Dong Y-H, Kvarnheden A, Yao J-L, Sutherland PW, Atkinson RG, Morris BAM, Gardner RC (1998) Identification of pollination-induced genes from the ovary of apple (Malus domestica). Sex Plant Reprod 11:277–283
Duggan DJ, Bittner M, Chen Y, Meltzer P, Trent JM (1999) Expression profiling using cDNA microarrays. Nat Genet 21:10–14
Gao ZS, van de Weg WE, Schaart JG, van der Meer IM, Kodde L, Laimer M, Breiteneder H, Hoffmann-Sommergruber K, Gilissen LJ (2005) Linkage map positions and allelic diversity of two Mal d 3 (non-specific lipid transfer protein) genes in the cultivated apple (Malus domestica). Theor Appl Genet 110:479–491
Gillaspy G, Ben-David H, Gruissem W (1993) Fruit: a developmental perspective. Plant Cell 5:1439–1451
Ito T, Kim GT, Shinozaki K (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J 22:257–264
Joanin P, Gigot C, Phillips G (1993) cDNA nucleotide sequence and expression of a maize cytoplasmic ribosomal protein S13 gene. Plant Mol Biol 21:701–704
John ME, Crow LJ (1992) Gene expression in cotton (Gossypium hirsutum L.) fiber: cloning of the mRNAs. Proc Natl Acad Sci USA 89:5769–5773
Kende H, Bradford K, Brummell D, Cho HT, Cosgrove D, Fleming A, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek LA (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314
Koning AJ, Tanimoto EY, Kiehne K, Rost T, Comai L (1991) Cell-specific expression of plant histone H2A genes. Plant Cell 3:657–665
König R, Baldessari D, Pollet N, Niehrs C, Eils R (2004) Reliability of gene expression ratios for cDNA microarrays in multiconditional experiments with a reference design. Nucleic Acids Res 32:e29
Lemaire-Chamley M, Petit J, Garcia V, Just D, Baldet P, Germain V, Fagard M, Mouassite M, Cheniclet C, Rothan C (2005) Changes in transcriptional profiles are associated with early fruit tissue specialization in tomato. Plant Physiol 139:750–769
Ludevid D, Hofte H, Himelblau E, Chrispeels MJ (1992) The expression pattern of the tonoplast intrinsic protein γ-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol 100:1633–1639
Maurel C, Chrespeels MJ (2001) Aquaporins. A molecular entry into plant water relations. Plant Physiol 125:135–138
Moyle R, Fairbairn DJ, Ripi J, Crowe M, Botella JR (2005) Developing pineapple fruit has a small transcriptome dominated by metallothionin. J Exp Bot 56:101–112
Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EH, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJ, Walton EF, Yauk YK (2006) Analyses of expressed sequence tags from apple. Plant Physiol 141:147–166
Pastorello EA, Pompei C, Pravettoni V, Brenna O, Farioli L, Trambaioli C, Conti A (2001) Lipid transfer proteins and 2S albumins as allergens. Allergy 67:45–47
Percy AE, O’Brien IEW, Jameson PE, Melton LD, MacRae EA, Redgewell RJ (1996) Xyloglucan endotransglycosylase activity during fruit development and ripening of apple and kiwifruit. Physiol Plant 96:43–50
Piechulla B, Pichersky E, Cashmore A, Gruissem W (1986) Expression of nuclear and plastid genes for photosynthesis-specific proteins during tomato fruit development and ripening. Plant Mol Biol 7:367–376
Piechulla B, Glick R, Bahl H, Melis A, Gruissem W (1987) Changes in photosynthetic capacity and photosynthetic protein pattern during tomato fruit ripening. Plant Physiol 84:911–917
Rohrer JR, Robertson KR, Phipps JB (1991) Variation in structure among fruits of Maloideae (Rosaceae). Am J Bot 78:1617–1635
Ruan Y, Gilmore J, Conner T (1998) Towards Arabidopsis genome analysis: monitoring expression profiles of 1400 genes using cDNA microarrays. Plant J 15:821–833
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, New York
Schena M, Shalon D, Heller R, Chai A, Brown PO, Davis RW (1996) Parallel human genome analysis: microarray based expression monitoring of 1000 genes. Proc Natl Acad Sci USA 93:10614–10619
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72
Singh AK, McIntyre LM, Sherman LA (2003) Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the Cyanobacterium, Synechocystis sp. PCC 6803. Plant Physiol 132:1825–1839
Sugita M, Gruissem W (1987) Developmental, organ-specific, and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family. Proc Natl Acad Sci USA 84:7104–7108
Szick K, Springer M, Bailey-Serres J (1998) Evolutionary analyses of the 12-kDa acidic ribosomal P-proteins reveal a distinct protein of higher plant ribosomes. Proc Natl Acad Sci USA 95:2378–2383
Tsugeki R, Kochieva EZ, Fedoroff NV (1996) A transposon insertion in the Arabidopsis SSR16 gene causes an embryo-defective lethal mutation. Plant J 10:479–489
Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388
Wanner L, Gruissem W (1991) Expression dynamics of the tomato rbcS gene family during development. Plant Cell 3:1289–1303
Zurek DM, Clouse SD (1994) Molecular cloning and characterization of a brassinosteroid-regulated gene from elongating soybean (Glycine max L.) epicotyls. Plant Physiol 104:161–170
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This work was supported by a grant from BioGreen21 Program, Rural Development Administration, Republic of Korea.
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Communicated by J.R. Liu.
Young-Pyo Lee and Gyung-Hee Yu contributed equally to this work.
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Lee, YP., Yu, GH., Seo, Y.S. et al. Microarray analysis of apple gene expression engaged in early fruit development. Plant Cell Rep 26, 917–926 (2007). https://doi.org/10.1007/s00299-007-0308-9
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DOI: https://doi.org/10.1007/s00299-007-0308-9