Skip to main content
Log in

Gene flow among different teosinte taxa and into the domesticated maize gene pool

  • Research Article
  • Published:
Genetic Resources and Crop Evolution Aims and scope Submit manuscript

Abstract

Maize (Zea mays L. ssp. mays) was domesticated from one wild species ancestor, the Balsas teosinte (Zea mays ssp. parviglumis) about 9000 years ago. Higher levels of gene diversity are found in teosinte taxa compared to maize, following domestication and selection bottlenecks. Diversity in maize can be increased via gene flow from teosinte, which has certainly occurred from various taxa, but the rate of flow from different teosinte taxa and the final impact on maize evolution has been difficult to measure. One hundred populations from six Zea taxa, both domesticated (maize) and wild (teosinte), including domesticated landraces from Asia, Africa, and the Americas, were genotyped with 17 SSR markers using 15 individuals per population. Overall levels of diversity were high, and populations could be distinguished based on markers. Relationships between populations followed most published reports, or can now help resolve previously conflicting reports. Gene flow into maize from different teosinte groups, and gene flow between different teosintes, was estimated. Evidence for contributions from the Balsas teosintes and from Chalco teosintes (Z. mays ssp. mexicana) to the maize gene pool was found, as well as from Chalco into ssp. mexicana race “Durango” and Z. mays ssp. huehuetenengensis. These contributions are almost certainly the result of post-domestication (and ongoing) exchanges. This information must give more impetus to in situ conservation of teosinte species, and use of these teosintes to continue to direct the evolution of maize, especially in response to new diseases, insect pests, and other biotic and abiotic stresses.

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

Similar content being viewed by others

References

  • Allen JO, Emenhiser GK, Kermicle JL (1989) Miniature kernel and plant: interaction between teosinte cytoplasmic genomes and maize nuclear genomes. Maydica 34:277–290

    Google Scholar 

  • Amusan IO, Richi PJ, Menkir A, Housley T, Ejeta G (2008) Resistance to Striga hermonthica in a maize inbred line derived from Zea diploperennis. New Phyt 178:157–166

    Article  Google Scholar 

  • Baltazar BM, Sanchez Gonzalez JJ, de la Cruz-Larios L, Schoper JB (2005) Pollination between maize and teosinte: an important determinant of gene flow in Mexico. Theor App Genet 110:519–526

    Article  Google Scholar 

  • Beadle GW (1932) Studies of Euchlaena and its hybrids with Zea. I. Chromosome behavior in Euchlaena mexicana and its hybrids with Zea mays. Die Zygodactylie und ihre Vererbung 62:291–304

    Google Scholar 

  • Beadle GW (1939) Teosinte and the origin of maize. J Hered 30:245–247

    Google Scholar 

  • Bellon MR, Berthaud J, Smale M, Aguirre JA, Taba S, Aragon F, Diaz J, Castro H (2003) Participatory landrace selection for on-farm conservation: an example from the Central Valleys of Oaxaca, Mexico. Genet Res Crop Evol 50:401–416

    Article  Google Scholar 

  • Benz BF, Sanchez-Velasquez LR, Santana Michel FJ (1990) Ecology and ethnobotany of Zea diploperennis: preliminary investigations. Maydica 35:85–98

    Google Scholar 

  • Blancas L, Arias DM, Ellstrand NC (2002) Patterns of genetic diversity in sympatric and allopatric populations of maize and its wild relative teosinte in Mexico: evidence for hybridization. In: Snow A (ed) Scientific methods workshop: ecological and agronomic consequences of gene flow from transgenic crops to wild relatives. Ohio State University, Columbus, pp 31–38

    Google Scholar 

  • Buckler ES, Holtsford TP (1996) Zea systematics: ribosomal ITS evidence. Mol Biol Evol 13:612–622

    Article  PubMed  CAS  Google Scholar 

  • Buckler ES, Stevens NM (2005) Maize origins, domestication and selection. In: Motley TJ, Zerega N, Cross HB (eds) Darwin’s Harvest. New approaches to the origins, evolution, and conservation of crops. Columbia University Press, NY

    Google Scholar 

  • Buckler ES, Thornsberry JM, Kresovich S (2001) Molecular diversity, structure and domestication of grasses. Genet Res 77:213–218

    Article  PubMed  CAS  Google Scholar 

  • Buckler ES, Gaut BS, McMullen MD (2006) Molecular and functional diversity of maize. Curr Op Plant Biol 9:172–176

    Article  CAS  Google Scholar 

  • Collins GN (1919) Structure of the maize ear as indicated in Zea-Euchlaena hybrids. J Ag Res 17:127–135

    Google Scholar 

  • Doebley JF (1990) Molecular evidence and the evolution of maize. Econ Bot 44:6–27

    Article  CAS  Google Scholar 

  • Doebley J (2004) The genetics of maize evolution. Ann Rev Gen 38:37–59

    Article  CAS  Google Scholar 

  • Doebley JF, Goodman MM, Stuber CW (1984) Isoenzymatic variation in Zea (Gramineae). Sys Bot 9:203–218

    Article  Google Scholar 

  • Doebley J, Renfroe W, Blanton A (1987) Restriction site variation in the Zea chloroplast genome. Genetics 117:139–147

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dubreuil P, Warburton M, Chastanet M, Hoisington D, Charcosset A (2006) More on the introduction of temperate maize into Europe: large-scale bulk SSR genotyping and new historical elements. Maydica 51:281–291

    Google Scholar 

  • Ellstrand NC, Garner LC, Hegde S, Guadagnuolo R, Blancas L (2007) Spontaneous hybridization between maize and teosinte. J Hered 98:183–187

    Article  PubMed  CAS  Google Scholar 

  • Emerson RA, Beadle GW (1932) Studies of Euchlaena and its hybrids with Zea. II. Crossing over between the chromosomes of Euchlaena and those of Zea. Z für induk Abst Vererb 30:5–15

    Google Scholar 

  • Eubanks MW (2001) The mysterious origin of maize. Econ Bot 55:492–514

    Article  Google Scholar 

  • Evans MMS, Kermicle JL (2001) Teosinte crossing barrier1, a locus governing hybridization of teosinte with maize. Theor Appl Genet 103:259–265

    Article  CAS  Google Scholar 

  • Eyre-Walker A, Gaut RL, Hilton H, Feldman DL, Gaut BS (1998) Investigation of the bottleneck leading to the domestication of maize. Proc Nat Acad Sci 95:4441–4446

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Franco J, Warburton M, Dubreuil P, Dreisigacker S (2005) User’s Manual for the FREQS-R Program for estimating allele frequencies for fingerprinting and genetic diversity studies using bulked heterogeneous populations. CIMMYT, Mexico, DF

    Google Scholar 

  • Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sanchez J, Liu L, Buckler ES, Doebley J (2005) Genetic diversity and population structure of teosinte. Genetics 169:2241–2254

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gauthier P, Gousenard B, Dallard J, Redaelli R, Rebourg C, Charcosset A, Boyat A (2002) RFLP diversity and relationships among traditional European maize populations. Theor Appl Genet 105:91–99

    Article  PubMed  CAS  Google Scholar 

  • Hamblin MT, Warburton ML, Buckler ES (2007) Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. PLoS One doi:10.1371/journal.pone.0001367

  • Iltis HH (1983) From teosinte to maize: the catastrophic sexual transmutation. Science 222:886–894

    Article  PubMed  CAS  Google Scholar 

  • Kato TA (1976) Cytological studies of maize (Zea mays L.) and teosinte (Zea mexicana (Schrader) Kuntze) in relation to their origin and evolution. Mass Ag Exp Sta Bull 635:1–186

    Google Scholar 

  • Kato TA (1984) Chromosome morphology and the origin of maize and it’s races. In MK Hecht et al. (eds) Evolutionary Biology, New York, pp 219-253

  • Kato TA, Mapes C, Mera LM, Serratos JA, Bye RA (2009) Origen y diversificación del maíz: una revisión analítica. Universidad Nacional Autónoma de México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Mexico, DF

  • Langham I (1956) Botanical gardens in ancient Mexico. Ann Mo Bo Garden 44:17–31

    Google Scholar 

  • Liu J, Muse SV (2005) PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129

    Article  PubMed  CAS  Google Scholar 

  • Longley AE (1941) Chromosome morphology in maize and its relatives. Bot Rev 7:263–289

    Article  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez J, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Nat Acad Sci 99:6080–6084

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Menkir A, Kling JG, Badu-Apraku B, Ibikunle O (2006) Registration of 26 tropical maize germplasm lines with resistance to Striga hermonthica. Crop Sci 46:1007–1009

    Article  Google Scholar 

  • Nuttall Z (1925) The gardens of ancient Mexico. Ann Rep Smithsonian Inst 1923:453–464

    Google Scholar 

  • Perrier X, Jacquemoud-Collet JP (2006) DARwin software http://darwin.cirad.fr/darwin

  • Piperno DR, Flannery KV (2001) The earliest archaeological maize (Zea mays L.) from highland Mexico: new accelerator mass spectrometry dates and their implications. Proc Nat Acad Sci 98:2101–2103

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pressoir G, Berthaud J (2004) Patterns of population structure in maize landraces from the Central Valleys of Oaxaca in Mexico. Heredity 92:88–94

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  PubMed Central  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Rebourg C, Chastanet M, Gouesnard B, Welcker C, Dubreuil P, Charcosset A (2003) Maize introduction into Europe: the history reviewed in the light of molecular data. Theor Appl Genet 106:895–903

    PubMed  CAS  Google Scholar 

  • Reif JC, Hamrit S, Heckenberger M, Schipprack W, Maurer HP, Bohn M, Melchinger AE (2005) Genetic structure and diversity of european flint maize populations determined with SSR analyses of individuals and bulks. Theor Appl Genet 111:906–913

    Article  PubMed  CAS  Google Scholar 

  • Ross-Ibarra R, Tenaillon M, Gaut BS (2009) Historical divergence and gene flow in the genus Zea. Genetics 181:1399–1413

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sanchez J, Kato TA, Aguilar M, Hernandez JM, Lopez A, Ruiz JA (1998) Distribución y caracterización del teocintle. Libro técnico 2. Instituto Nacional de Investigaciones Forestales. Agrícolas y Pecuarias, Jalisco, México

    Google Scholar 

  • SAS Institute Inc (2007) SAS OnlineDoc® 9.2. Cary, NC: SAS Institute Inc. USA

  • Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225

    Article  PubMed  CAS  Google Scholar 

  • Thuillet A, Tenaillon MI, Anderson MK, Mitchell SE, Kresovich S, Stack SM, Gaut B, Doebley J (2008) A weak effect of background selection on trinucleotide microsatellites in maize. J Hered 99:45–55

    Article  PubMed  CAS  Google Scholar 

  • Van Heerwaarden J, Ross-Ibarra J, Doebley J, Glaubitz JC, Sanchez Gonzalez JD, Gaut BS, Eguiarte LE (2010) Fine scale genetic structure in the wild ancestor of maize (Zea mays ssp. parviglumis). Mol Ecol 19:1162–1173

    Article  PubMed  Google Scholar 

  • Vigouroux Y, Glaubitz JC, Matsuoka Y, Goodman MM, Sánchez J, Doebley J (2008) Population structure and genetic diversity of new world maize races assessed by DNA microsatellites. Am J Bot 95:1240–1253

    Article  PubMed  Google Scholar 

  • Warburton ML, Reif JC, Frisch M, Bohn M, Bedoya C, Xia XC, Crossa J, Franco J, Hoisington D, Pixley K, Taba S, Melchinger AE (2008) Genetic diversity in CIMMYT nontemperate maize germplasm: landraces, open-pollinated varieties, and inbred lines. Crop Sci 48:617–624

    Article  Google Scholar 

  • Wellhausen EJ, Roberts LM, Hernández-Xolocotzi E (1952) Races of maize in México. Their origin, characteristics and distribution. Bussey Institution of Harvard University, Cambridge

    Google Scholar 

  • Wilkes HG (1967) Teosinte: The closest relative of maize. Bussey Institute, Harvard University, Cambridge

    Google Scholar 

  • Wilkes HG (1979) Mexico and Central America as a centre for the origin of agriculture and the evolution of maize. Crop Imp 6:16–18

    Google Scholar 

  • Wilkes HG (1996) El teocintle en México: Panorama retrospectivo y análisis personal. In: Serratos JA, Willcox MC, Castillo F (eds) Flujo genético entre maíz criollo, maíz mejorado y teocintle: implicaciones para el maíz transgénico. CIMMYT, México, DF

    Google Scholar 

  • Wilkes HG (2006) Urgent notice to all maize researchers: disappearance and extinction of the last wild teosinte populations is more than half completed. A modest proposal for teosinte evolution and conservation in situ: the Balsas, Guerrero, Mexico. Maydica 52:49–58

    Google Scholar 

Download references

Acknowledgments

The authors thank Drs. V. Mahalakshmi, A. Menkir, Z. Muthamia, S.H. Zhang, Sutrisno, M. Yunus, P. Grudloyma and P. X. Hao for providing maize landraces for the study; Drs. J. Crouch, L. George, M. Tenaillon, B. Baldwin and M. Sawkins for advice on the manuscript, and Mr. H. Chavez and Ms. V. Combes for expert laboratory technical work. Funding was received from the Generation Challenge Program of the Consultative Group on International Agriculture Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marilyn L. Warburton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Warburton, M.L., Wilkes, G., Taba, S. et al. Gene flow among different teosinte taxa and into the domesticated maize gene pool. Genet Resour Crop Evol 58, 1243–1261 (2011). https://doi.org/10.1007/s10722-010-9658-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10722-010-9658-1

Keywords

Navigation