Skip to main content
Log in

The amplification and evolution of orthologous 22-kDa α-prolamin tandemly arrayed genes in coix, sorghum and maize genomes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Tandemly arrayed genes (TAGs) account for about one-third of the duplicated genes in eukaryotic genomes. They provide raw genetic material for biological evolution, and play important roles in genome evolution. The 22-kDa prolamin genes in cereal genomes represent typical TAG organization, and provide the good material to investigate gene amplification of TAGs in closely related grass genomes. Here, we isolated and sequenced the Coix 22-kDa prolamin (coixin) gene cluster (283 kb), and carried out a comparative analysis with orthologous 22-kDa prolamin gene clusters from maize and sorghum. The 22-kDa prolamin gene clusters descended from orthologous ancestor genes, but underwent independent gene amplification paths after the separation of these species, therefore varied dramatically in sequence and organization. Our analysis indicated that the gene amplification model of 22-kDa prolamin gene clusters can be divided into three major stages. In the first stage, rare gene duplications occurred from the ancestor gene copy accidentally. In the second stage, rounds of gene amplification occurred by unequal crossing over to form tandem gene array(s). In the third stage, gene array was further diverged by other genomic activities, such as transposon insertions, segmental rearrangements, etc. Unlike their highly conserved sequences, the amplified 22-kDa prolamin genes diverged rapidly at their expression capacities and expression levels. Such processes had no apparent correlation to age or order of amplified genes within TAG cluster, suggesting a fast evolving nature of TAGs after gene amplification. These results provided insights into the amplification and evolution of TAG families in grasses.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

TAGs:

Tandemly arrayed genes

UCO:

Unequal crossing over

TEs:

Transposable elements

LTR:

Long terminal repeat

MITEs:

Miniature inverted repeat transposable elements

SINEs:

Short interspersed repetitive elements

mya:

Million years ago

References

  • Arora RK (1977) Job’s-tears (coix lacryma-jobi)—a minor food and fodder crop of northeastern India. Econ Bot 31:358–366

    Google Scholar 

  • Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL (2007) Patterns in grass genome evolution. Curr Opin Plant Biol 10:176–181

    Article  CAS  PubMed  Google Scholar 

  • Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13:137–144

    Article  CAS  PubMed  Google Scholar 

  • Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    Article  CAS  PubMed  Google Scholar 

  • Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360

    Article  CAS  PubMed  Google Scholar 

  • Clarke BC, Mukai Y, Appels R (1996) The Sec-1 locus on the short arm of chromosome 1R of rye (Secale cereale). Chromosoma 105:269–275

    CAS  PubMed  Google Scholar 

  • Clayton WD (1983) Notes on the tribe Andropogoneae (Gramineae). Kew Bull 35:813–818

    Article  Google Scholar 

  • Clayton WD, Renvoize SA (1986) Genera Graminum. Grasses of the world. Her Majesty’s Stationery Office, London

    Google Scholar 

  • DeRose RT, Ma DP, Kwon IS, Hasnain SE, Klassy RC, Hall TC (1989) Characterization of the kafirin gene family from sorghum reveals extensive homology with zein from maize. Plant Mol Biol 12:245–256

    Article  CAS  Google Scholar 

  • Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  CAS  PubMed  Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    CAS  PubMed  Google Scholar 

  • Feng L, Zhu J, Wang G, Tang Y, Chen H, Jin W, Wang F, Mei B, Xu Z, Song R (2009) Expressional profiling study revealed unique expressional patterns and dramatic expressional divergence of maize alpha-zein super gene family. Plant Mol Biol 69:649–659

    Article  CAS  PubMed  Google Scholar 

  • Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99:9573–9578

    CAS  PubMed  Google Scholar 

  • Gao S, Gu YQ, Wu J, Coleman-Derr D, Huo N, Crossman C, Jia J, Zuo Q, Ren Z, Anderson OD et al (2007) Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 65:189–203

    Article  CAS  PubMed  Google Scholar 

  • Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28

    Article  CAS  Google Scholar 

  • Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94:6809–6814

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  CAS  PubMed  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202

    CAS  PubMed  Google Scholar 

  • Gu YQ, Crossman C, Kong X, Luo M, You FM, Coleman-Derr D, Dubcovsky J, Anderson OD (2004) Genomic organization of the complex alpha-gliadin gene loci in wheat. Theor Appl Genet 109:648–657

    Article  CAS  PubMed  Google Scholar 

  • Hallauer AR, Miranda JB (1988) Quantitative genetics in maize breeding. Iowa State University Press, Ames, IA

    Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Kawaura K, Mochida K, Ogihara Y (2005) Expression profile of two storage-protein gene families in hexaploid wheat revealed by large-scale analysis of expressed sequence tags. Plant Physiol 139:1870–1880

    Article  PubMed  Google Scholar 

  • Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205

    Article  CAS  PubMed  Google Scholar 

  • Kim WT, Okita TW (1988) Structure, expression, and heterogeneity of the rice seed prolamines. Plant Physiol 88:649–655

    Article  CAS  PubMed  Google Scholar 

  • Lai J, Li Y, Messing J, Dooner HK (2005) Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci USA 102:9068–9073

    Article  CAS  PubMed  Google Scholar 

  • Li WH, Gu Z, Wang H, Nekrutenko A (2001) Evolutionary analyses of the human genome. Nature 409:847–849

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Ouyang S, Egan A, Nobuta K, Haas BJ, Zhu W, Gu X, Silva JC, Meyers BC, Buell CR (2008) Characterization of paralogous protein families in rice. BMC Plant Biol 8:18

    Article  PubMed  Google Scholar 

  • Lisch D, Chomet P, Freeling M (1995) Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics 139:1777–1796

    CAS  PubMed  Google Scholar 

  • Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410

    Article  CAS  PubMed  Google Scholar 

  • Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102:5454–5459

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Huang B, Zhou L, He Y, Chen Q, Yuan Y, Xu Z, Song R (2010) Construction of a Coix BAC library and isolation of the 22 kDa α-coixin gene cluster. Genome 53:667–674

    Article  CAS  PubMed  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF et al (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354

    Article  CAS  PubMed  Google Scholar 

  • Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Heidelberg, Germany

    Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437

    Article  CAS  PubMed  Google Scholar 

  • Ottoboni LM, Leite A, Yunes JA, Targon ML, de Souza Filho GA, Arruda P (1993) Sequence analysis of 22 kDa-like alpha-coixin genes and their comparison with homologous zein and kafirin genes reveals highly conserved protein structure and regulatory elements. Plant Mol Biol 21:765–778

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908

    Article  CAS  PubMed  Google Scholar 

  • Rizzon C, Ponger L, Gaut BS (2006) Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol 2:e115

    Article  PubMed  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  CAS  PubMed  Google Scholar 

  • Semple C, Wolfe KH (1999) Gene duplication and gene conversion in the Caenorhabditis elegans genome. J Mol Evol 48:555–564

    Article  CAS  PubMed  Google Scholar 

  • Shantz HL (1954) The place of grasslands in the earth’s cover of vegetation. Ecology 35:143–145

    Article  Google Scholar 

  • Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627–13632

    Article  CAS  PubMed  Google Scholar 

  • Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science 191:528–535

    Article  CAS  PubMed  Google Scholar 

  • Song R, Messing J (2002) Contiguous genomic DNA sequence comprising the 19-kD zein gene family from maize. Plant Physiol 130:1626–1635

    Article  CAS  PubMed  Google Scholar 

  • Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060

    Article  CAS  PubMed  Google Scholar 

  • Song R, Llaca V, Linton E, Messing J (2001) Sequence, regulation, and evolution of the maize 22-kD alpha zein gene family. Genome Res 11:1817–1825

    CAS  PubMed  Google Scholar 

  • Song R, Llaca V, Messing J (2002) Mosaic organization of orthologous sequences in grass genomes. Genome Res 12:1549–1555

    Article  CAS  PubMed  Google Scholar 

  • Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Tsubota SI, Rosenberg D, Szostak H, Rubin D, Schedl P (1989) The cloning of the Bar region and the B breakpoint in Drosophila melanogaster: evidence for a transposon-induced rearrangement. Genetics 122:881–890

    CAS  PubMed  Google Scholar 

  • Veit B, Vollbrecht E, Mathern J, Hake S (1990) A tandem duplication causes the Kn1-O allele of Knotted, a dominant morphological mutant of maize. Genetics 125:623–631

    CAS  PubMed  Google Scholar 

  • Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117

    Article  CAS  PubMed  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  CAS  PubMed  Google Scholar 

  • Xu JH, Messing J (2008) Organization of the prolamin gene family provides insight into the evolution of the maize genome and gene duplications in grass species. Proc Natl Acad Sci USA 105:14330–14335

    Article  CAS  PubMed  Google Scholar 

  • Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor Appl Genet 119:1397–1412

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Wang H (2007) LTR—FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265–W268

    Article  PubMed  Google Scholar 

  • Yandeau-Nelson MD, Xia Y, Li J, Neuffer MG, Schnable PS (2006) Unequal sister chromatid and homolog recombination at a tandem duplication of the A1 locus in maize. Genetics 173:2211–2226

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C et al (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  Google Scholar 

  • Zhang L, Gaut BS (2003) Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res 13:2533–2540

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like thank Yiwei Yuan for technical support on sequencing analysis, Yuanping Tang for sequence analysis. This work was supported by National Natural Sciences Foundation of China (30671303, 30700472), Ministry of Education of China (NCET-06-0435, 206048), Ministry of Science and Technology of China (2006AA10Z148, 2006AA10A107, 2009CB118400), Fok Ying Tung Education Foundation (101024), Science and Technology Commission of Shanghai Municipality (05PJ14049, 05QMX1424, 09DZ2271800), Education Commission of Shanghai Municipality (05ZZ02), and Shanghai Education Foundation (04SG40).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rentao Song.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 185 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, L., Huang, B., Meng, X. et al. The amplification and evolution of orthologous 22-kDa α-prolamin tandemly arrayed genes in coix, sorghum and maize genomes. Plant Mol Biol 74, 631–643 (2010). https://doi.org/10.1007/s11103-010-9705-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9705-5

Keywords

Navigation