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Genomic isolation of genes encoding starch branching enzyme II (SBEII) in apple: toward characterization of evolutionary disparity in SbeII genes between monocots and eudicots

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Abstract

Two genes encoding starch branching enzyme II (SBEII) have been identified in apple. These genes share 94 and 92% identity in coding DNA sequences and amino acid sequences, respectively; moreover, they have similar expression patterns. Both genes are expressed in vegetative and reproductive tissues, including leaves, buds, flowers, and fruits. Based on genomic Southern blots, there are two copies of SbeII genes in the apple genome. Comparisons of genomic sequences between monocots and eudicots have revealed that the genomic structure of SbeII genes is conserved. However, the 5′-terminal region of coding DNA sequences of SbeII genes shows greater divergence than the 3′-terminal region between monocots and eudicots. Phylogenetic analysis of DNA sequences has demonstrated that the duplication patterns of SbeII genes are different between monocots and eudicots. In monocots, the duplication of SbeII genes must have occurred prior to the radiation of grasses (Poaceae); while, in eudicots, the expansion of SbeII genes must have followed the process of speciation.

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References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Båga M, Glaze S, Mallard CS, Chibbar RN (1999) A starch-branching enzyme gene in wheat produces alternatively spliced transcripts. Plant Mol Biol 40:1019–1030

    Article  PubMed  Google Scholar 

  • Båga M, Nair RB, Repellin A, Scoles GJ, Chibbar RN (2000) Isolation of a cDNA encoding a granule-bound 152-kilodalton starch-branching enzyme in wheat1. Plant Physiol 124:253–264

    Article  PubMed  Google Scholar 

  • Baguma Y, Sun C, Ahlandsberg S, Mutisya J, Palmqvist S, Rubaihayo PR, Magambo MJ, Egwange TG, Larsson H, Jansson C (2003) Expression patterns of the gene encoding starch branching enzyme II in the storage roots of cassava (Manihot esculenta Crantz). Plant Sci 164:833–839

    Article  CAS  Google Scholar 

  • Ball SG, van de Wal MHBJ, Visser RGF (1998) Progress in understanding the biosynthesis of amylose. Trends Plant Sci 3:462–467

    Article  Google Scholar 

  • Blauth SL, Yao Y, Klucinec JD, Shannon JC, Thompson DB, Guiltinan MJ (2001) Identification of mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol 125:1396–1405

    Article  PubMed  CAS  Google Scholar 

  • Boyer CD, Preiss J (1978) Multiple forms of (1→4)-α-d-glucan, (1→4)-α-d-glucan-6-glycosyl transferase from developing Zea mays L. kernels. Carbohydr Res 61:321–334

    Article  CAS  Google Scholar 

  • Burton RA, Bewley JD, Smith AM, Bhattacharyya MK, Tatge H, Ring S, Bull V, Hamilton WDO, Martin C (1995) Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J 7:3–15

    Article  PubMed  CAS  Google Scholar 

  • Chaw S, Chang C, Chen H, Li W (2004) Dating the monocot–dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441

    Article  PubMed  CAS  Google Scholar 

  • Chevreau E, Lespinasse Y, Gallet M (1985) Inheritance of pollen enzymes and polyploid origin of apple (Malus × domestica Borkh.) Theor Appl Genet 71:268–277

    CAS  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA mini-preparation, version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Dumez S, Wattebled F, Dauvillee D, Delvalle D, Planchot V, Ball SG, D’Hulst C (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 18:2694–2709

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fisher DK, Gao M, Kim KN, Boyer CD, Guiltinan MJ (1996) Two closely related cDNAs encoding starch branching enzyme from Arabidopsis thaliana. Plant Mol Biol 30:97–108

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Fisher DK, Kim K, Shannon JC, Guiltinan MJ (1997) Independent genetic control of maize starch-branching enzymes IIa and IIb: isolation and characterization of Sbe2a cDNA. Plant Physiol 114:69–78

    Article  PubMed  CAS  Google Scholar 

  • Guan H, Preiss J (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiol 102:1269–1273

    PubMed  CAS  Google Scholar 

  • Hamada S, Nozaki K, Ito H, Yoshimoto Y, Yoshida H, Hiraga S, Onodera S, Honma M, Takeda Y, Matsui H (2001) Two starch-branching-enzyme isoforms occur in different fractions of developing seeds of kidney bean. Biochem J 359:23–34

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Gasic K, Sun F, Xu M, Korban SS (2007a) A gene encoding starching branching enzyme I (SBEI) in apple (Malus × domestica, Rosaceae) and its phylogenetic relationship to Sbe genes from other angiosperms. Mol Phylogenet Evol 43:852–863. doi:10.1016/j.ympev.2006.09.00

    Google Scholar 

  • Han Y, Gasic K, Marron B, Beever JE, Korban SS (2007b) A BAC-based physical map of the apple genome. Genomics 89:630–637

    Article  PubMed  CAS  Google Scholar 

  • Hong S, Preiss J (2000) Localization of C-terminal domains required for the maximal activity or for determination of substrate preference of maize branching enzymes. Arch Biochem Biophys 378:349–355

    Article  PubMed  CAS  Google Scholar 

  • Hong S, Mikkelsen R, Preiss J (2001) Analysis of the amino terminus of maize branching enzyme II by polymerase chain reaction random mutagenesis. Arch Biochem Biophys 386:62–68

    Article  PubMed  CAS  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  PubMed  CAS  Google Scholar 

  • Jobling SA, Schwall GP, Westcott RJ, Sidebottom CM, Debet M, Gidley MJ, Jeffcoat R, Safford R (1999) A minor form of starch branching enzyme in potato (Solanum tuberosum L.) tubers has a major effect on starch structure: cloning and characterization of multiple forms of SBE A. Plant J 18:163–171

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki T, Mizuno K, Baba T, Shimada H (1993) Molecular analysis of the gene encoding a rice starch branching enzyme. Mol Gen Genet 237:10–16

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Fisher DK, Gao M, Guiltinan MJ (1998a) Genomic organization and promoter activity of the maize starch branching enzyme I gene. Gene 216:233–243

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Fisher DK, Gao M, Guiltinan MJ (1998b) Molecular cloning and characterization of the Amylose-Extender gene encoding starch branching enzyme IIB in maize. Plant Mol Biol 38:945–956

    Article  PubMed  CAS  Google Scholar 

  • Kuriki T, Stewart DC, Preiss J (1997) Construction of chimeric enzymes out of maize endosperm branching enzymes i and ii: activity and properties. J Biol Chem 272:28999–29004

    Article  PubMed  CAS  Google Scholar 

  • Larsson CT, Khoshnoodi J, Ek B, Rask L, Larsson H (1998) Molecular cloning and characterization of starch-branching enzyme II from potato. Plant Mol Biol 37:505–511

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Mizuno K, Kimura K, Arai Y, Kawasaki T, Shimada H, Baba T (1992) Starch branching enzymes from immature rice seeds. J Biochem 112:643–651

    PubMed  CAS  Google Scholar 

  • Morell MK, Blennow A, Kosar-Hashemi B, Samuel MS (1997) Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiol 113:201–208

    Article  PubMed  CAS  Google Scholar 

  • Mutisya J, Sathish P, Sun C, Andersson L, Ahlandsberg S, Baguma Y, Palmqvist S, Odhiambo B, Aman P, Jansson C (2003) Starch branching enzymes in sorghum (Sorghum bicolor) and barley (Hordeum vulgare): comparative analyses of enzyme structure and gene expression. J Plant Physiol 160:921–930

    Article  PubMed  CAS  Google Scholar 

  • Myers AM, Morell MK, James MG, Ball SG (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol 122:989–997

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol 43:718–725

    Article  PubMed  CAS  Google Scholar 

  • Neuffer MG, Coe EH, Wessler SR (1997) Mutants of maize. Cold Spring Harbor Lab Press, Cold Spring Harbor, p 124

    Google Scholar 

  • Newcomb RE, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJF, Walton EF, Yauk YK (2006) Analysis of expressed sequence tags from apple. Plant Physiol 141:147–166

    Article  PubMed  Google Scholar 

  • Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol 127:459–472

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, New York

    Google Scholar 

  • Rahman S, Regina A, Li Z, Mukai Y, Yamamoto M, Hashemi BK, Abrahams S, Morell MK (2001) Comparison of starch branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch branching enzyme IIa from the wheat D genome donor Aegilops tauschii. Plant Physiol 125:1314–1324

    Article  PubMed  CAS  Google Scholar 

  • Regina A, Kosar-Hashemi B, Li Z, Pedler A, Mukai Y, Yamamoto M, Gale K, Sharp PJ, Morell MK, Rahman S (2005) Starch branching enzyme IIb in wheat is expressed at low levels in the endosperm compared to other cereals and encoded at a non-syntenic locus. Planta 222:899–909

    Article  PubMed  CAS  Google Scholar 

  • Sun C, Sathish P, Ahlandsberg S, Deiber A, Jansson C (1997) Identification of four starch-branching enzymes in barley endosperm: partial purification of forms I, IIa, and IIb. New Phytol 137:215–222

    Article  CAS  Google Scholar 

  • Sun C, Sathish P, Ahlandsberg S, Jansson C (1998) The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol 118:37–49

    Article  PubMed  CAS  Google Scholar 

  • Suzuki G, Moriyama M, Fujioka K, Yamamoto M, Subrahmanyam NC, Li Z, Appels R, Morell M, Mukai Y, Rahman S (2003) The starch branching enzyme I locus from Aegilops tauschii, the donor of the D genome to wheat. Funct Integr Genomics 3:69–75

    PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland

  • Takeda Y, Guan HP, Preiss J (1993) Branching of amylase by the branching isoenzymes of maize endosperm. Carbohydr Res 240:253–263

    Article  CAS  Google Scholar 

  • Tatum T, Stepanovic S, Biradar DP, Rayburn AL, Korban SS (2005) Variation in nuclear DNA content in Malus species and cultivated apples. Genome 48:924–930

    PubMed  CAS  Google Scholar 

  • Xu M, Song J, Cheng Z, Jiang J, Korban SS (2001) A bacterial artificial chromosome (BAC) library of Malus floribunda 821 and contig construction for positional cloning of the apple scab resistance gene Vf. Genome 44:1104–1113

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Korban SS, Song J, Jiang J (2002) Constructing a bacterial artificial chromosome library of the apple cultivar GoldRush. Acta Hort 595:103–112

    CAS  Google Scholar 

  • Yamanouchi H, Nakamura Y (1992) Organ specificity of isoforms of starch branching enzyme (Q-enzyme) in rice. Plant Cell Physiol 33:985–991

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by funds received from the USDA Cooperative State Research, Education and Extension Service—National Research Initiative—Plant Genome Program grant No. 2005-35300-15538. Also, funding was received from the University of Illinois Office of Research.

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Authors and Affiliations

  1. Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, 61801, USA

    Yuepeng Han, Elise Bendik, Ksenija Gasic & Schuyler S. Korban

  2. Department of Crop Sciences, University of Illinois, Urbana, IL, 61801, USA

    Feng-Jie Sun

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  1. Yuepeng Han
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  2. Elise Bendik
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  4. Ksenija Gasic
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  5. Schuyler S. Korban
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Correspondence to Schuyler S. Korban.

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Han, Y., Bendik, E., Sun, FJ. et al. Genomic isolation of genes encoding starch branching enzyme II (SBEII) in apple: toward characterization of evolutionary disparity in SbeII genes between monocots and eudicots. Planta 226, 1265–1276 (2007). https://doi.org/10.1007/s00425-007-0555-6

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