Skip to main content
SpringerLink
Log in

Molecular evidence for post-domestication selection in the Waxy gene of Chinese waxy maize

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Waxy maize was first reported in China in 1909 and is mainly used in food production in Asia. The evidence for strong domestication selection in the Waxy locus of rice and a selective sweep around its genomic region make us to wonder whether there has been similar selection in Waxy in glutinous maize. To address this issue, DNA sequences of Waxy, three flanking genes and an unlinked gene (Adh1) of 30 accessions sampled from Chinese waxy maize accessions, including representative landraces and inbred lines, were determined in this study. Sharp reduction of nucleotide diversity and significant neutrality tests (Tajima’s D and Fu and Li’s F*) were observed in the Waxy locus in Chinese waxy maize but not in nonglutinous maize; comparison with the unlinked gene confirmed that this pattern was different to Waxy. Sequence analysis across a 143 kb genomic segment centered on the Waxy locus revealed patterns consistent with a selective sweep in the upstream region of Waxy. The selective sweep detected based on current limited genomic sequences exceeded over 50 kb, indicating strong selection in this or a bigger region. However, No sweep effect was detected in the repetitive downstream region of Waxy. Phylogenetic analysis indicated that Chinese waxy maize was domesticated from the cultivated flint maize (Zea mays ssp. mays) that was introduced from the new world. At least two independent deletions in exon 7 (30 bp) and 10 (15 bp) were identified in the Chinese accessions respectively. These findings demonstrate a similar pattern of domestication selection in the Waxy genomic region in both glutinous maize and rice, suggesting that this pattern in the rise of glutinous phenotype is likely in other cereal crops.

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
Fig. 4

Similar content being viewed by others

References

  • Cao ZB, Xu WW (1990) On maize race. China Seeds 4: 7–9 (in Chinese)

    Google Scholar 

  • Collins GN (1909) A new type of Indian corn from China. Bur of Plant Ind (Bulletin) 161:1–30

    Google Scholar 

  • Collins GN (1920) Waxy maize from upper Burma. Science 52:48–51

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Gaut BS, Clegg MT (1993) Molecular evolution of the Adh1 locus in the genus Zea. Proc Natl Acad Sci USA 90:5095–5099

    Article  PubMed  CAS  Google Scholar 

  • Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294

    Article  PubMed  CAS  Google Scholar 

  • Huang YB, Rong TZ (1998) Genetic diversity and origin of Chinese waxy maize. Crop J upl:77–80 (in Chinese)

    Google Scholar 

  • Institute of Crop Germplasm Resources, Chinese Academy of Agricultural Science and Institute of Maize, Shandong Academy of Agricultural Science (1988) Maize cultivars in China. Chinese Agriculture Press, Beijing (in Chinese)

    Google Scholar 

  • Jugenheimer RW (1976) Corn: improvement, seed production and uses. John Wiley & Sons, Inc., New York

    Google Scholar 

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

    Article  Google Scholar 

  • Kuleshov NN (1954) Some peculiarities in the maize of Asia. Ann Mo Bot Gard 41:271–299

    Article  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Marillonnet S, Wessler SR (1997) Retrotranspson insertion into the maize waxy gene results in tissue-specific RNA processing. Plant Cell 9:967–978

    Article  PubMed  CAS  Google Scholar 

  • National Standards of the People’s Republic of China (GB–T17891) (1999) China Standard Press, Beijing (in Chinese)

  • Okagaki RJ, Neuffer MG, Wessler SR (1991) A deletion common to two independently derived waxy mutations of maize. Genetics 128:425–431

    PubMed  CAS  Google Scholar 

  • Olsen KM, Purugganan MD (2002) Molecular evidence on the origin and evolution of glutinous rice. Genetics 162:941–950

    PubMed  CAS  Google Scholar 

  • Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan MD (2006) Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173:975–983

    Article  PubMed  CAS  Google Scholar 

  • Palaisa K, Morgante M, Tingey S, Rafalski A (2004) Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc Natl Acad Sci USA 101:9885–9890

    Article  PubMed  CAS  Google Scholar 

  • Patron NJ, Smith AM, Fahy BF, Hylton CM, Naldrett MJ, Rossnagel BG, Denyer K (2002) The altered pattern of amylose accumulation in the endosperm of low-amylose barley cultivars is attributable to a single mutation allele of granule-bound starch synthase I with a deletion in the 5′-non-coding region. Plant Physiol 130:190–198

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-De I, Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Saito M, Nakamura T (2005) Two point mutations identified in emmer wheat generate null Wx-A1 alleles. Theor Appl Genet 110:276–282

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (1989) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press

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

    Article  CAS  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9166

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tiffin P, Gaut BS (2001) Sequence diversity in the tetraploid Zea perennis and the closely related diploid Z. diploperennis: insights from four nuclear loci. Genetics 158:401–412

    PubMed  CAS  Google Scholar 

  • Vrinten P, Nakamura T, Yamamori M (1999) Molecular characterization of waxy mutations in wheat. Mol Gen Genet 261:463–71

    Article  PubMed  CAS  Google Scholar 

  • Wang RL, Stec A, Hey J, Lukens L, Doebley J (1999) The limits of selection during maize domestication. Nature 398:236–239

    Article  PubMed  CAS  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276

    Article  PubMed  CAS  Google Scholar 

  • Weatherwax P (1955) Early history of corn and theories as to its origin. In: Sprague GF (ed) Corn and corn improvement. Academic Press, New York, pp 1–16

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wessler SR, Tarpley A, Purugganan M, Spell M, Okagaki R (1990) Filler DNA is associated with spontaneous deletions in maize. Proc Natl Acad Sci USA 87:8731–8735

    Article  PubMed  CAS  Google Scholar 

  • Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES (2002) Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA 99:12959–12962

    Article  PubMed  CAS  Google Scholar 

  • Zeng M (1987) Blood relationship of Chinese waxy maize. Crop Germplasm Resources 3:21–24 (in Chinese)

    Google Scholar 

  • Zeng M, Liu Y (1994) Origin of Chinese waxy maize (Zea mays sinensis). Maize Genetics Cooperation Newsletter (MNL) 68:12

    Google Scholar 

  • Zeng M, Yang T, Wang P (1981) The relative analyses on maize cultivar Menghai Four-row Wax. Act Genetica Sinica 8:91–96 (in Chinese with English abstract)

    Google Scholar 

  • Zhang L, Peek AS, Dunams D, Gaut BS (2002) Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics 162:851–860

    PubMed  CAS  Google Scholar 

  • Zhu Q, Zhang X, Luo J, Gaut BS, Ge S (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol Biol Evol 24:875–888

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. William Hill (University of Edinburgh) and Dr. Qian-Hao Zhu (CSIRO) for their critical reading of the manuscript, Dianxin Wu (Zhejiang University) for assistance in determination of amylose content and Jingqin Zhu (Zhejiang Academy of Agricultural Science) for maize accessions. This work was supported by the National Basic Research Program of China (973 Program) (2008CB117002) to LF.

Author information

Authors and Affiliations

  1. Institute of Crop Science, Zhejiang University, Hangzhou, 310029, China

    Longjiang Fan, Liyan Quan, Xiaodong Leng, Xingyi Guo & Weiming Hu

  2. Institute of Bioinformatics, Zhejiang University, Hangzhou, 310029, China

    Longjiang Fan & Xingyi Guo

  3. Institute of Biotechnology, Hangzhou Academy of Agricultural Science, Hangzhou, 310024, China

    Songlin Ruan & Huasheng Ma

  4. Institute of Genetics and Developmental Biology, Chinese Academy of Science, Beijing, 100101, China

    Mengqian Zeng

Authors
  1. Longjiang Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liyan Quan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaodong Leng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingyi Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weiming Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Songlin Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huasheng Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mengqian Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Longjiang Fan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fan, L., Quan, L., Leng, X. et al. Molecular evidence for post-domestication selection in the Waxy gene of Chinese waxy maize. Mol Breeding 22, 329–338 (2008). https://doi.org/10.1007/s11032-008-9178-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-008-9178-2

Keywords

Search

Navigation