Skip to main content
Log in

Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Polyploidization has repeatedly occurred during plant evolution. Although autopolyploidy is the best model to characterize the polyploidization effects in a highly controlled manner, there are limited studies on autopolyploids compared to allopolyploids. To improve our understanding of autopolyploidy effects in maize, we developed an inbred Oh43 ploidy series consisting of the diploid (2X), tetraploid (4X) and hexaploid (6X) lines and compared their phenotypes and gene expression in the mature adult leaf tissue. Our phenotypic study showed that plants of higher ploidy exhibit increased cell size but slower growth rate, later flowering, fewer tassel branches, reduced stature and fertility. Two-dimensional difference gel electrophoresis (2D DIGE) and gel electrophoresis followed by liquid chromatography and mass spectrometry (GeLC-MS) assays of the leaf proteomes revealed ~40 and 26% quantitative differentially expressed (DE) proteins, respectively, at the per genome level. A small number of qualitative DE proteins were also identified in the GeLC-MS assay. The majority of the quantitative DE proteins found in the 2D DIGE assay were present in either the 4X versus 6X or the 2X versus 6X comparison but not the 2X versus 4X comparison. Aneuploidy in some 6X plants might contribute to the more extensive changes of gene expression per genome in the 6X. Most changes of the protein expression per genome are less than twofold. Less than 5% of the DE genes exhibit a positive or negative continuous correlation through the ploidy series between their protein expression per genome, and the genome copy number. Hence, in the Oh43 ploidy series, expression for most proteins in a cell increases linearly with ploidy.

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

Similar content being viewed by others

References

  • Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4:2072–2081

    Article  CAS  PubMed  Google Scholar 

  • Abel S, Becker HC (2007) The effect of autopolyploidy on biomass production in homozygous lines of Brassica rapa and Brassica oleracea. Plant Breed 126:642–643

    Article  Google Scholar 

  • Albertin W, Brabant P, Catrice O, Eber F, Jenczewski E, Chèvre AM, Thiellement H (2005) Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics 5:2131–2139

    Article  CAS  PubMed  Google Scholar 

  • Andrews DL, MacAlpine DM, Johnson JR, Kelley PM, Cobb BG, Drew MC (1994) Differential induction of mRNAs for the glycolytic and ethanolic fermentative pathways by hypoxia and anoxia in maize seedlings. Plant Physiol 106:1575–1582

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Auger DL, Gray AD, Ream TS, Kato A, Coe EH Jr, Birchler JA (2005) Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 169:389–397

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA (1981) The genetic basis of dosage compensation of alcohol dehydrogenase-1 in maize. Genetics 97:625–637

    CAS  PubMed  Google Scholar 

  • Birchler JA (2010) Reflections on studies of gene expression in aneuploids. Biochem J 426:119–123

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Newton KJ (1981) Modulation of protein levels in chromosomal dosage series of maize: the biochemical basis of aneuploid syndromes. Genetics 99:247–266

    CAS  PubMed  Google Scholar 

  • Blakeslee AF (1934) New Jimson weeds from old chromosomes. J Hered 24:80–108

    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 

  • Christie PJ, Alfenito MR, Walbot V (2004) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 94:541–549

    Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  CAS  PubMed  Google Scholar 

  • Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172

    Article  CAS  PubMed  Google Scholar 

  • d’Erfuth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R (2009) Turning meiosis into mitosis. PLoS Biol 7:e1000124

    Article  Google Scholar 

  • Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461

    Article  CAS  PubMed  Google Scholar 

  • Espartero J, Pintor-Toro JA, Pardo JM (1994) Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227

    Article  CAS  PubMed  Google Scholar 

  • Ferris R, Taylor G (1994) Stomatal characteristics of four native herbs following exposure to elevated CO2. Ann Bot 73:447–453

    Article  CAS  Google Scholar 

  • Ferris R, Long L, Bunn SM, Robinson KM, Bradshaw HD, Rae AM, Taylor G (2002) Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiol 22:633–640

    CAS  PubMed  Google Scholar 

  • Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR (1999) Ploidy regulation of gene expression. Science 285:251–254

    Article  CAS  PubMed  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 

  • Giri AP, Wünsche H, Mitra S, Zavala JA, Muck A, Svatos A, Baldwin IT (2006) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VII. Changes in the plant’s proteome. Plant Physiol 142:1621–1641

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gómez J, Sánchez-Martínez D, Stiefel V, Rigau J, Puigdomènech P, Pagès M (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334:262–264

    Article  PubMed  Google Scholar 

  • Groose RW, Talbert LE, Kojis WP, Bingham ET (1989) Progressive heterosis in autotetraploid alfalfa: studies using two types of inbreds. Crop Sci 29:1173–1177

    Article  Google Scholar 

  • Guo M, Davis D, Birchler JA (1996) Dosage effects on gene expression in a maize ploidy series. Genetics 142:1349–1355

    CAS  PubMed  Google Scholar 

  • Havlis J, Thomas H, Sebela M, Shevchenko A (2003) Fast-response proteomics by accelerated in-gel digestion of proteins. Anal Chem 75:1300–1306

    Article  CAS  PubMed  Google Scholar 

  • Hegarty MJ, Hiscock SJ (2008) Genomic clues to the evolutionary success of polyploidy plants. Curr Biol 18:435–444

    Article  Google Scholar 

  • Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81:802–806

    Article  CAS  PubMed  Google Scholar 

  • Jiménez CR, Huang L, Qiu Y, Burlingame AL (1998) In-gel digestion of proteins for MALDI-MS fingerprint mapping. In: Coligan JE (ed) Current protocols in protein science. Wiley, Brooklyn, pp 1641–1645

    Google Scholar 

  • Kasprzewska A (2003) Plant chitinases—regulation and function. Cell Mol Biol Lett 8:809–824

    CAS  PubMed  Google Scholar 

  • Kato A (1997) Induced single fertilization in maize. Sex Plant Reprod 10:96–100

    Article  Google Scholar 

  • Kato A (1999a) Induction of bicellular pollen by trifluralin treatment and occurrence of triploids and aneuploids after fertilization in maize. Genome 42:154–157

    Article  Google Scholar 

  • Kato A (1999b) Air drying method using nitrous oxide for chromosome counting in maize. Biotech Histochem 74:160–166

    Article  CAS  PubMed  Google Scholar 

  • Kato A, Birchler JA (2006) Induction of tetraploid derivatives of maize inbred lines by nitrous oxide gas treatment. J Hered 97:39–44

    Article  CAS  PubMed  Google Scholar 

  • Kato A, Albert P, Vega JM, Birchler JA (2006) Sensitive FISH signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem 81:71–78

    Article  PubMed  Google Scholar 

  • Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25

    Article  Google Scholar 

  • Levings CS, Dudley JW, Alexander DE (1967) Inbreeding and crossing in autotetraploid maize. Crop Sci 7:72–73

    Article  Google Scholar 

  • Levy AA, Feldman M (2002) The impact of polyploidy on grass genome evolution. Plant Physiol 130:1587–1593

    Article  CAS  PubMed  Google Scholar 

  • Martelotto LG, Ortiz JPA, Stein J, Espinoza F, Quarin CL, Pessino SC (2005) A comprehensive analysis of gene expression alterations in a newly synthesized Paspalum notatum autotetraploid. Plant Sci 169:211–220

    Article  CAS  Google Scholar 

  • Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424

    Article  CAS  PubMed  Google Scholar 

  • Mok DWS, Peloquin SJ (1975) Breeding value of 2n pollen (diploandroids) in tetraploid x diploid crosses in potato. Theor Appl Genet 46:307–314

    Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed  Google Scholar 

  • Randolph LF (1942) The influence of heterozygosis on fertility and vigor in autotetraploid maize. Genetics 27:163

    Google Scholar 

  • Rhoades MM, Dempsey E (1966) Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics 54:505–522

    CAS  PubMed  Google Scholar 

  • Riddle NC, Kato A, Birchler JA (2006) Genetic variation for the response to ploidy change in Zea mays L. Theor Appl Genet 114:101–111

    Article  PubMed  Google Scholar 

  • Riddle NC, Jiang H, An L, Doerge RW, Birchler JA (2010) Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet 120:341–353

    Article  CAS  PubMed  Google Scholar 

  • Rose JK, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Selvi MT, Sharma R (1999) Sunlight-induced anthocyanin pigmentation in maize vegetative tissues. J Exp Bot 50:1619–1625

    Article  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Tate JA (2003) Advances in the study of polyploidy since plant speciation. New Phytol 161:173–191

    Article  Google Scholar 

  • Stebbins GL Jr (1940) The significance of polyploidy in plant evolution. Am Nat 74:54–66

    Article  Google Scholar 

  • Stupar RM, Bhaskar PB, Yandell BS, Rensink WA, Hart AL, Ouyang S, Veilleux RE, Busse JS, Erhardt RJ, Buell CR, Jiang J (2007) Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176:2055–2067

    Article  CAS  PubMed  Google Scholar 

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  Google Scholar 

  • Yu Z, Haberer G, Matthes M, Rattei T, Mayer KF, Gierl A, Torres-Ruiz RA (2010) Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc Natl Acad Sci USA 107:17809–17814

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Roy J. Lowery (Charles W. Gehrke Proteomics Center, University of Missouri-Columbia) for assistance with the 2D DIGE analysis. This research was funded by NSF plant genome grant DBI0733857.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James A. Birchler.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yao, H., Kato, A., Mooney, B. et al. Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol Biol 75, 237–251 (2011). https://doi.org/10.1007/s11103-010-9722-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9722-4

Keywords

Navigation