Natural variation in teosinte at the domestication locus teosinte branched1 (tb1)

Premise of the study: The teosinte branched1 (tb1) gene is a major QTL controlling branching differences between maize and its wild progenitor, teosinte. The insertion of a transposable element (Hopscotch) upstream of tb1 is known to enhance the gene’s expression, causing reduced tillering in maize. Observations of the maize tb1 allele in teosinte and estimates of an insertion age of the Hopscotch that predates domestication led us to investigate its prevalence and potential role in teosinte. Methods: Prevalence of the Hopscotch element was assessed across an Americas-wide sample of 1110 maize and teosinte individuals using a co-dominant PCR assay. Population genetic summaries were calculated for a subset of individuals from four teosinte populations in central Mexico. Phenotypic data were also collected from a single teosinte population where Hopscotch was found segregating. Key results: Genotyping results suggest the Hopscotch element is at higher than expected frequency in teosinte. Analysis of linkage disequilibrium near tb1 does not support recent introgression of the Hopscotch allele from maize into teosinte. Population genetic signatures are consistent with selection on this locus revealing a potential ecological role for Hopscotch in teosinte. Finally, two greenhouse experiments with teosinte do not suggest tb1 controls tillering in natural populations. Conclusions: Our findings suggest the role of Hopscotch differs between maize and teosinte. Future work should assess tb1 expression levels in teosinte with and without the Hopscotch and more comprehensively phenotype teosinte to assess the ecological significance of the Hopscotch insertion and, more broadly, the tb1 locus in teosinte.

[1]  Katherine E. Guill,et al.  The Genomic Impacts of Drift and Selection for Hybrid Performance in Maize , 2013, Genetics.

[2]  K. Olsen,et al.  A bountiful harvest: genomic insights into crop domestication phenotypes. , 2013, Annual review of plant biology.

[3]  M. Hufford,et al.  Teosinte as a model system for population and ecological genomics. , 2012, Trends in genetics : TIG.

[4]  M. Hufford,et al.  The Genomic Signature of Crop-Wild Introgression in Maize , 2012, PLoS genetics.

[5]  M. Hufford,et al.  Complex Patterns of Local Adaptation in Teosinte , 2012, Genome biology and evolution.

[6]  J. Doebley,et al.  Evidence for a Natural Allelic Series at the Maize Domestication Locus teosinte branched1 , 2012, Genetics.

[7]  M. Netea,et al.  Low prevalence of lactase persistence in Neolithic South-West Europe , 2012, European Journal of Human Genetics.

[8]  Xun Xu,et al.  Comparative population genomics of maize domestication and improvement , 2012, Nature Genetics.

[9]  Peter J. Bradbury,et al.  Maize HapMap2 identifies extant variation from a genome in flux , 2012, Nature Genetics.

[10]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[11]  A. Flavell,et al.  Islands and streams: clusters and gene flow in wild barley populations from the Levant , 2012, Molecular ecology.

[12]  Jeffrey Ross-Ibarra,et al.  Genetic Architecture of Maize Kernel Composition in the Nested Association Mapping and Inbred Association Panels1[W] , 2011, Plant Physiology.

[13]  Jeffrey Ross-Ibarra,et al.  Identification of a functional transposon insertion in the maize domestication gene tb1 , 2011, Nature Genetics.

[14]  Fang Yang,et al.  grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses , 2011, Proceedings of the National Academy of Sciences.

[15]  S. Dreisigacker,et al.  Gene flow among different teosinte taxa and into the domesticated maize gene pool , 2011, Genetic Resources and Crop Evolution.

[16]  J. Doebley,et al.  Genetic signals of origin, spread, and introgression in a large sample of maize landraces , 2010, Proceedings of the National Academy of Sciences.

[17]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[18]  K. Olsen,et al.  Genetic perspectives on crop domestication. , 2010, Trends in plant science.

[19]  David B. Witonsky,et al.  Using Environmental Correlations to Identify Loci Underlying Local Adaptation , 2010, Genetics.

[20]  K. Olsen,et al.  Molecular evolution of shattering loci in U.S. weedy rice , 2010, Molecular ecology.

[21]  C. Ridley,et al.  Crops gone wild: evolution of weeds and invasives from domesticated ancestors , 2010, Evolutionary applications.

[22]  E. Vollbrecht,et al.  Evidence of selection at the ramosa1 locus during maize domestication , 2010, Molecular ecology.

[23]  Qihui Zhu,et al.  Selection on grain shattering genes and rates of rice domestication. , 2009, The New phytologist.

[24]  M. Scott,et al.  Wide variability in kernel composition, seed characteristics, and zein profiles among diverse maize inbreds, landraces, and teosinte , 2009, Theoretical and Applied Genetics.

[25]  B. Gaut,et al.  Historical Divergence and Gene Flow in the Genus Zea , 2009, Genetics.

[26]  D. Piperno,et al.  Starch grain and phytolith evidence for early ninth millennium B.P. maize from the Central Balsas River Valley, Mexico , 2009, Proceedings of the National Academy of Sciences.

[27]  Takanori Nakano,et al.  Reverse Evolution of Armor Plates in the Threespine Stickleback , 2008, Current Biology.

[28]  M. Kovach,et al.  Leveraging natural diversity: back through the bottleneck. , 2008, Current opinion in plant biology.

[29]  L. Rieseberg,et al.  Selection on domestication traits and quantitative trait loci in crop–wild sunflower hybrids , 2007, Molecular ecology.

[30]  Richard M. Clark,et al.  Major Regulatory Genes in Maize Contribute to Standing Variation in Teosinte (Zea mays ssp. parviglumis) , 2007, Genetics.

[31]  Brandon S Gaut,et al.  Linkage Mapping of Domestication Loci in a Large Maize–Teosinte Backcross Resource , 2007, Genetics.

[32]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[33]  T. Brutnell,et al.  The molecular analysis of the shade avoidance syndrome in the grasses has begun. , 2007, Journal of experimental botany.

[34]  Yuling Bai,et al.  Domestication and Breeding of Tomatoes: What have We Gained and What Can We Gain in the Future? , 2007, Annals of botany.

[35]  P. Tiffin,et al.  Population Structure and Its Effects on Patterns of Nucleotide Polymorphism in Teosinte (Zea mays ssp. parviglumis) , 2007, Genetics.

[36]  B. Gaut,et al.  Plant domestication, a unique opportunity to identify the genetic basis of adaptation , 2007, Proceedings of the National Academy of Sciences.

[37]  N. Ellstrand,et al.  Spontaneous hybridization between maize and teosinte. , 2007, The Journal of heredity.

[38]  Richard M. Clark,et al.  A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture , 2006, Nature Genetics.

[39]  Paul Scheet,et al.  A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. , 2006, American journal of human genetics.

[40]  Steven G. Schroeder,et al.  The Effects of Artificial Selection on the Maize Genome , 2005, Science.

[41]  J. Doebley,et al.  Genetic Diversity and Population Structure of Teosinte , 2005, Genetics.

[42]  Jeremy Schmutz,et al.  Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles , 2005, Science.

[43]  J. Goudet.  HIERFSTAT , a package for R to compute and test hierarchical F -statistics , 2005 .

[44]  J. Doebley,et al.  The role of barren stalk1 in the architecture of maize , 2004, Nature.

[45]  J. Doebley.  The genetics of maize evolution. , 2004, Annual review of genetics.

[46]  Kevin Thornton,et al.  libsequence: a C++ class library for evolutionary genetic analysis , 2003, Bioinform..

[47]  V. Gavrilovic,et al.  Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[49]  J. Doebley,et al.  A single domestication for maize shown by multilocus microsatellite genotyping , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Richard R. Hudson,et al.  Generating samples under a Wright-Fisher neutral model of genetic variation , 2002, Bioinform..

[51]  John Doebley,et al.  Epistatic and environmental interactions for quantitative trait loci involved in maize evolution , 1999 .

[52]  Honor C. Prentice,et al.  Gene Flow and Introgression from Domesticated Plants into Their Wild Relatives , 1999 .

[53]  L. Rieseberg,et al.  The persistence of cultivar alleles in wild populations of sunflowers five generations after hybridization , 1997, Theoretical and Applied Genetics.

[54]  J. Doebley,et al.  The evolution of apical dominance in maize , 1997, Nature.

[55]  J. Doebley,et al.  teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. , 1995, Genetics.

[56]  J. Doebley,et al.  Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. , 1993, Genetics.

[57]  J. Doebley,et al.  Genetic analysis of the morphological differences between maize and teosinte. , 1991, Genetics.

[58]  R. Jorgensen,et al.  Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[59]  S. Barrett.  Crop mimicry in weeds , 1983, Economic Botany.

[60]  H. G. Wllkes.  Hybridization of maize and teosinte, in mexico and guatemala and the improvement of maize , 1977, Economic Botany.

[61]  Wei Li.  Tassels replace upper ears1 encodes a putative transcription factor that regulates maize shoot architecture by multiple pathways , 2012 .

[62]  M. Netea,et al.  Low prevalence of lactase persistence in Neolithic , 2012 .

[63]  M. Hufford.  Genetic and ecological approaches to guide conservation of teosinte (Zea mays ssp. parviglumis), the wild progenitor of maize , 2010 .

[64]  H. Velthuizen,et al.  Harmonized World Soil Database (version 1.2) , 2008 .

[65]  Holly M. Mortensen,et al.  Convergent adaptation of human lactase persistence in Africa and Europe , 2007, Nature Genetics.

[66]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[67]  T. Ogihara,et al.  [Linkage mapping]. , 1996, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[68]  J. Doyle,et al.  A rapid DNA isolation procedure for small amounts of fresh leaf tissue , 1987 .