Skip to main content
SpringerLink
Log in

Waxy strains of three amaranth grains raised by different mutations in the coding region

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Waxy strains raised by waxy mutation have been found for three amaranth grains. Three genes encoding waxy protein were isolated from Amaranthus caudatus (Wx-ca), A. cruentus (Wx-cr), and A. hypochondriacus (Wx-hy). Sequence analysis indicated that the Wx-ca, Wx-cr, and Wx-hy genes contained the same exon (13 exons) and intron (12 introns) structure. The lengths of the Wx-ca, Wx-cr, and Wx-hy genes were 3,236, 3,237, and 3,225 bp, respectively. The alignment of the coding sequence of the three Waxy genes showed 12 polymorphic sites, including 11 single nucleotide polymorphisms (SNPs) (in exons 10 and 12 and introns 1, 3, 4, 9, and 11) and 5 deletions or insertions (indels) (in introns 4, 9, and 11). In particular, major polymorphism was detected in 8- and 3-bp indels in intron 4. Moreover, the mutation in the waxy alleles (wx-ca, wx-cr, and wx-hy) of all three species was also isolated and characterized. Comparison of coding sequences of the three Waxy genes and their waxy alleles indicated one base insertion (wx-ca: insert of T base in exon 8) and a base substitution (wx-cr: a G-to-T base substitution in exon 10; wx-hy: a G-to-A base substitution in exon 6), which occurred as internal termination codon in the three Waxy genes, suggesting the involvement of a nonsense or frameshift mutation. Therefore, these different mutations in coding regions were considered to be the cause of the waxy (amylose-free) phenotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ainsworth C, Gale M, Baird S (1983) The genetics of β-amylase isozymes in wheat. Theor Appl Genet 66:39–49

    Article  CAS  Google Scholar 

  • Arciga-Reyes L, Wootton L, Kieffer M, Davies B (2006) UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in arabidopsis. Plant J 47:480–489

    Article  CAS  PubMed  Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Article  CAS  PubMed  Google Scholar 

  • Breene W (1991) Food uses of grain amaranth. Cereal Foods World 36:426–430

    CAS  Google Scholar 

  • Bureau T, Wessler S (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Cai X, Wang Z, Xing Y, Zhang J, Hong M (1998) Aberrant splicing of intron 1 leads to the heterogeneous 5’UTR and decreased expression of waxy gene in rice cultivars of intermediate amylose content. Plant J 14:459–465

    Article  CAS  PubMed  Google Scholar 

  • Camirand A, St-Pierre B, Marineau C, Brisson N (1990) Occurrence of a copia-like transposable element in one of the introns of the potato starch phosphorylase gene. Mol Gen Genet 224:33–39

    Article  CAS  PubMed  Google Scholar 

  • Campbell WH, Gowri G (1990) Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol 92:1–11

    Article  CAS  PubMed  Google Scholar 

  • Chan KF, Sun M (1997) Genetic diversity detected by isozyme and RAPD analysis of crop and wild species of amaranthus. Theor Appl Genet 95:865–873

    Article  CAS  Google Scholar 

  • Clark J, Robertson M, Ainsworth C (1991) Nucleotide sequence of a wheat (Triticum aestivum L.) cDNA clone encoding the waxy protein. Plant Mol Biol 16:1099–1101

    Article  CAS  PubMed  Google Scholar 

  • Costea M, Sanders A, Waines G (2001) Preliminary results toward a revision of the Amaranthus hybridus species complex (Amaranthaceae). Sida 19:931–974

    Google Scholar 

  • Costea M, Brenner DM, Tardif FJ, Tan YF, Sun M (2006) Delimitation of Amaranthus cruentus L. and Amaranthus caudatus L. using micromorphology and AFLP analysis: an application in germplasm identification. Genet Resour Crop Evol 53:1625–1633

    Article  Google Scholar 

  • Davis J, Supatcharee N, Khandellwal R, Chibbar R (2003) Synthesis of novel starches in Planta: opportunities and challenges. Starch/Staerke 55:107–120

    Article  CAS  Google Scholar 

  • Domon E, Fujita M, Ishikawa N (2002a) The insertion/deletion polymorphisms in the waxy gene of barley genetic resources from East Asia. Theor Appl Genet 104:132–138

    Article  CAS  PubMed  Google Scholar 

  • Domon E, Saito A, Takeda K (2002b) Comparison of the waxy locus sequence from a non-waxy strain and two waxy mutants of spontaneous and artificial origins in barley. Genes Genet Syst 77:351–359

    Article  CAS  PubMed  Google Scholar 

  • Dry I, Smith A, Edward A, Bhattacharyya M, Dunn P, Martin C (1992) Characterization of cDNAs encoding two isoforms of granule-bound starch synthase which show differential expression in developing storage organs of pea and potato. Plant J 2:193–202

    CAS  PubMed  Google Scholar 

  • Echt C, Schwartz D (1981) Evidence for the inclusion of controlling elements within the structural gene at the waxy locus in maize. Genetics 99:275–284

    CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978

    Article  CAS  PubMed  Google Scholar 

  • Fedoroff N, Wessler S, Shure M (1983) Isolation of the transposable maize controlling elements Ac and Ds. Cell 35:235–242

    Article  CAS  PubMed  Google Scholar 

  • Fukunaga K, Kawase M, Kato K (2002) Structural variation in the Waxy gene and differentiation in foxtail millet [Setaria italica (L.) P. Beauv.]: implications for multiple origins of the waxy phenotype. Mol Genet Genomics 268:214–222

    Article  CAS  PubMed  Google Scholar 

  • Furukawa K, Tagaya M, Inouye M, Preiss J, Fukui T (1990) Identification of lysine 15 at the active site in Escherichia coli glycogen synthase. Conservation of Lys-X-Gly-Gly sequence in the bacterial and mammalian enzymes. J Biol Chem 265:2086–2090

    CAS  PubMed  Google Scholar 

  • Hirano HY, Eiguchi M, Sano Y (1998) A single base change altered the regulation of the waxy gene at the posttranscriptional level during the domestication of rice. Mol Biol Evol 15:978–987

    CAS  PubMed  Google Scholar 

  • Hovenkamp-Hermelink J, Jacobsen E, Ponstein A, Visser R, Vos-Scheperkeuter G, Bijmolt E, Vries J, Witholt B, Feenstra W (1987) Isolation of an amylose-free starch mutant of the potato (Solanum tuberosum L.). Theor Appl Genet 75:217–221

    Article  Google Scholar 

  • Hseih J (1988) Genetic studies of the Wx gene of sorghum (Sorghum bicolor [L.] Moench). Bot Bull Academia Sinica 29:293–299

    Google Scholar 

  • Hsieh J, Liu C, Hsing Y (1996) Molecular cloning of a sorghum cDNA encoding the seed waxy protein. Plant Physiol 112:1735

    Article  Google Scholar 

  • Inouchi N, Nishi K, Tanaka S, Asai M, Kawase Y, Hata Y, Konishi Y, Yue S, Fuwa H (1999) Characterization of amaranth and quinoa starches. J Appl Glycosci 46:233–240

    CAS  Google Scholar 

  • Isshiki M, Yamamoto Y, Satoh H, Shimamoto K (2001) Nonsense-mediated decay of mutant waxy mRNA in rice. Plant Physiol 125:1388–1395

    Article  CAS  PubMed  Google Scholar 

  • Juan R, Pastor J, Alaiz M, Vioque J (2007) Electrophoretic characterization of Amaranthus L. seed proteins and its systematic implications. Bot J Linn Soc 155:57–63

    Article  Google Scholar 

  • Kawase M, Fukunaga K, Kato K (2005) Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Mol Genet Genomics 274:131–140

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kimura T, Ideta O, Saito A (2000) Identification of the gene encoding granule-bound starch synthase I in sweet potato (Ipomoea batatas (L.) Lam.). Plant Biotechnol 17:247–252

    CAS  Google Scholar 

  • Klosgen R, Gierl A, Schwarz-Sommer Z, Saedler H (1986) Molecular analysis of the waxy locus of Zea mays. Mol Genet Genomics 203:237–244

    Article  Google Scholar 

  • Konishi Y, Nojima H, Okuno K, Asaoka M, Fuwa H (1985) Characterization of starch granules from waxy, nonwaxy, and hybrid seeds of Amaranthus hypochondriacus L. Agri Biol Chem 49:1965–1971

    CAS  Google Scholar 

  • Kumar A, Larsen C, Preiss J (1986) Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli ADP-glucose: alpha-1, 4-glucan, 4-glucosyltransferase as deduced from the nucleotide sequence of the glgA gene. J Biol Chem 261:16256–16259

    CAS  PubMed  Google Scholar 

  • Lanoue KZ, Wolf PG, Browning S, Hood EE (1996) Phylogenetic analysis of restriction-site variation in wild and cultivated Amaranthus species (Amaranthaceae). Theor Appl Genet 93:722–732

    Article  CAS  Google Scholar 

  • Marcone M (2001) Starch properties of Amaranthus pumilus (seabeach amaranth): a threatened plant species with potential benefits for the breeding/amelioration of present Amaranthus cultivars. Food Chem 73:61–66

    Article  CAS  Google Scholar 

  • Mochizuki K, Umeda M, Ohtsubo H, Ohtsubo E (1992) Characterization of a plant SINE, p-SINE1, in rice genomes. Jpn J Genet 67:155–166

    Article  CAS  PubMed  Google Scholar 

  • Murai J, Taira T, Ohta D (1999) Isolation and characterization of the three waxy genes encoding the granule-bound starch synthase in hexaploid wheat. Gene 234:71–79

    Article  CAS  PubMed  Google Scholar 

  • Murray M, Thompson W (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4325

    Google Scholar 

  • Nakamura T, Vrinten P, Hayakawa K, Ikeda J (1998) Characterization of a granule-bound starch synthase isoform found in the pericarp of wheat. Plant Physiol 118:451–459

    Article  CAS  PubMed  Google Scholar 

  • Nakayama H, Afzal M, Okuno K (1998) Intraspecific differentiation and geographical distribution of Wx alleles for low amylose content in endosperm of foxtail millet, Setaria italica (L.) Beauv. Euphytica 102:289–293

    Article  Google Scholar 

  • Nelson O, Rines H (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300

    Article  CAS  PubMed  Google Scholar 

  • Okagaki R (1992) Nucleotide sequence of a long cDNA from the rice waxy gene. Plant Mol Biol 19:513–516

    Article  CAS  PubMed  Google Scholar 

  • Okuno K, Sakaguchi S (1981) Glutinous and non-glutinous starches in perisperm of grain amaranths. Cereal Res Commun 9:305–310

    CAS  Google Scholar 

  • Okuno K, Sakaguchi S (1982) Inheritance of starch characteristics in perisperm of Amaranthus hypochondriacus. J Hered 73:467

    Google Scholar 

  • Park YJ, Nemoto K, Nishikawa T, Matsushima K, Minami M, Kawase M (2009) Molecular cloning and characterization of granule bound starch synthase I cDNA from a grain amaranth (Amaranthus cruentus L.). Breed Sci (in press)

  • Rohde W, Becker D, Salamini F (1988) Structural analysis of the waxy locus from Hordeum vulgare. Nucl Acids Res 16:7185

    Article  CAS  PubMed  Google Scholar 

  • Salehuzzaman S, Jacobsen E, Visser R (1993) Isolation and characterization of a cDNA encoding granule-bound starch synthase in cassava (Manihot esculenta Crantz) and its antisense expression in potato. Plant Mol Biol 23:947–962

    Article  CAS  PubMed  Google Scholar 

  • Sano Y (1984) Differential regulation of waxy gene expression in rice endosperm. Theor Appl Genet 68:467–473

    Article  CAS  Google Scholar 

  • Sauer JD (1950) The grain amaranths: a survey of their history and classification. Ann Missouri Bot Gard 37:561–619

    Article  Google Scholar 

  • Sauer JD (1967) The grain amaranths and their relatives: a revised taxonomic and geographic survey. Ann Missouri Bot Gard 54:103–137

    Article  Google Scholar 

  • Saunders R, Becker R (1984) Amaranthus: a potential food and feed resource. Adv Cereal Sci Technol 6:357–396

    CAS  Google Scholar 

  • Sprague G, Brimhall B, Hixon R (1943) Some effects of the waxy gene in corn on properties of the endosperm starch. J Am Soc Agron 35:817

    Google Scholar 

  • Sugimoto Y, Yamada K, Sakamoto S, Fuwa H (1981) Some properties of normal-and waxy-type starches of Amaranthus hypochondriacus L. pp 112–116

  • Swofford D (1988) PAUP*: phylogenetic analysis using parsimony and other methods, version 4.0 (test ver. 61–64). Sinauer Associates Publishers, Sunderland

  • Thompson JDG, Plewniak FJ, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Tsai C (1974) The function of the waxy locus in starch synthesis in maize endosperm. Biochem Genetics 11:83–96

    Article  CAS  Google Scholar 

  • van der Leij F, Visser R, Ponstein A, Jacobsen E, Feenstra W (1991) Sequence of the structural gene for granule-bound starch synthase of potato (Solanum tuberosum L.) and evidence for a single point deletion in the amf allele. Mol Gen Genet 228:240–248

    Article  PubMed  Google Scholar 

  • Van K, Onoda S, Kim MY, Kim KD, Lee SH (2008) Allelic variation of the Waxy gene in foxtail millet [Setaria italica (L.) P. Beauv.] by single nucleotide polymorphisms. Mol Genet Genom 279:255–266

    Article  CAS  Google Scholar 

  • Vrinten P, Nakamura T, Yamamori M (1999) Molecular characterization of waxy mutations in wheat. Mol Genet Genomics 261:463–471

    Article  CAS  Google Scholar 

  • Wang Z, Wu Z, Xing Y, Zheng F, Guo X, Zhang W, Hong M (1990) Nucleotide sequence of rice waxy gene. Nucl Acids Res 18:5898

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zheng F, Shen G, Gao J, Snustad D, Li M, Zhang J, Hong M (1995) The amylose content in rice endosperm is related to the post-transcriptional regulation of the waxy gene. Plant J 7:613–622

    Article  CAS  PubMed  Google Scholar 

  • Wessler S, Varagona M (1985) Molecular basis of mutations at the waxy locus of maize: correlation with the fine structure genetic map. Proc Natl Acad Sci 82:4177–4181

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Sun M (2001) Comparative analysis of phylogenetic relationships of grain amaranths and their wild relatives (Amaranthus; Amaranthaceae) using internal transcribedspacer, amplified fragment length polymorphism, and double-primer fluorescent intersimple sequence repeat markers. Mol Phylogenet Evol 21:372–387

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We express our sincere thanks to Dr. D. Brenner of USDA-ARS-MWA-PIRU; Iowa State University, USA, for providing the accessions used in this experiment.

Author information

Authors and Affiliations

  1. Department of Bioscience and Food Production Science, Interdisciplinary Graduate School of Science & Technology, Shinshu University, 8304 Minamiminowa, Nagano, 399-4598, Japan

    Young-Jun Park

  2. Graduate School of Agriculture, Shinshu University, 8304 Minamiminowa, Nagano, 399-4598, Japan

    Kazuhiro Nemoto, Kenichi Matsushima & Mineo Minami

  3. Genebank, National Institute of Agrobiological Sciences, 2-1-2 Tsukuba, Ibaraki, 305-8602, Japan

    Tomotaro Nishikawa & Makoto Kawase

Authors
  1. Young-Jun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuhiro Nemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomotaro Nishikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kenichi Matsushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mineo Minami
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Makoto Kawase
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young-Jun Park.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, YJ., Nemoto, K., Nishikawa, T. et al. Waxy strains of three amaranth grains raised by different mutations in the coding region. Mol Breeding 25, 623–635 (2010). https://doi.org/10.1007/s11032-009-9360-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-009-9360-1

Keywords

Search

Navigation