Publications by authors named "John F Doebley"

34 Publications

The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication.

PLoS Genet 2020 05 14;16(5):e1008791. Epub 2020 May 14.

Laboratory of Genetics, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

The genetics of domestication has been extensively studied ever since the rediscovery of Mendel's law of inheritance and much has been learned about the genetic control of trait differences between crops and their ancestors. Here, we ask how domestication has altered genetic architecture by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. We observed a strongly reduced number of QTL for domestication traits in maize relative to teosinte, which is consistent with the previously reported depletion of additive variance by selection during domestication. We also observed more dominance in maize than teosinte, likely a consequence of selective removal of additive variants. We observed that large effect QTL have low minor allele frequency (MAF) in both maize and teosinte. Regions of the genome that are strongly differentiated between teosinte and maize (high FST) explain less quantitative variation in maize than teosinte, suggesting that, in these regions, allelic variants were brought to (or near) fixation during domestication. We also observed that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of the additive variance in both teosinte and maize is "missing" in the sense that it cannot be ascribed to detectable QTL and only 25% of variance maps to specific QTL. This latter result suggests that morphological evolution during domestication is largely attributable to very large numbers of QTL of very small effect.
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http://dx.doi.org/10.1371/journal.pgen.1008791DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7266358PMC
May 2020

TeoNAM: A Nested Association Mapping Population for Domestication and Agronomic Trait Analysis in Maize.

Genetics 2019 11 3;213(3):1065-1078. Epub 2019 Sep 3.

Laboratory of Genetics, University of Wisconsin-Madison, Wisconsin 53706

Recombinant inbred lines (RILs) are an important resource for mapping genes controlling complex traits in many species. While RIL populations have been developed for maize, a maize RIL population with multiple teosinte inbred lines as parents has been lacking. Here, we report a teosinte nested association mapping (TeoNAM) population, derived from crossing five teosinte inbreds to the maize inbred line W22. The resulting 1257 BCS RILs were genotyped with 51,544 SNPs, providing a high-density genetic map with a length of 1540 cM. On average, each RIL is 15% homozygous teosinte and 8% heterozygous. We performed joint linkage mapping (JLM) and a genome-wide association study (GWAS) for 22 domestication and agronomic traits. A total of 255 QTL from JLM were identified, with many of these mapping near known genes or novel candidate genes. TeoNAM is a useful resource for QTL mapping for the discovery of novel allelic variation from teosinte. TeoNAM provides the first report that , a rice domestication gene, is also a QTL associated with tillering in teosinte and maize. We detected multiple QTL for flowering time and other traits for which the teosinte allele contributes to a more maize-like phenotype. Such QTL could be valuable in maize improvement.
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http://dx.doi.org/10.1534/genetics.119.302594DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6827374PMC
November 2019

The genome-wide dynamics of purging during selfing in maize.

Nat Plants 2019 09 2;5(9):980-990. Epub 2019 Sep 2.

Department of Ecology and Evolutionary Biology, UC Irvine, Irvine, CA, USA.

Self-fertilization (also known as selfing) is an important reproductive strategy in plants and a widely applied tool for plant genetics and plant breeding. Selfing can lead to inbreeding depression by uncovering recessive deleterious variants, unless these variants are purged by selection. Here we investigated the dynamics of purging in a set of eleven maize lines that were selfed for six generations. We show that heterozygous, putatively deleterious single nucleotide polymorphisms are preferentially lost from the genome during selfing. Deleterious single nucleotide polymorphisms were lost more rapidly in regions of high recombination, presumably because recombination increases the efficacy of selection by uncoupling linked variants. Overall, heterozygosity decreased more slowly than expected, by an estimated 35% to 40% per generation instead of the expected 50%, perhaps reflecting pervasive associative overdominance. Finally, three lines exhibited marked decreases in genome size due to the purging of transposable elements. Genome loss was more likely to occur for lineages that began with larger genomes with more transposable elements and chromosomal knobs. These three lines purged an average of 398 Mb from their genomes, an amount equivalent to three Arabidopsis thaliana genomes per lineage, in only a few generations.
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http://dx.doi.org/10.1038/s41477-019-0508-7DOI Listing
September 2019

Hybrid Decay: A Transgenerational Epigenetic Decline in Vigor and Viability Triggered in Backcross Populations of Teosinte with Maize.

Genetics 2019 09 18;213(1):143-160. Epub 2019 Jul 18.

Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706

In the course of generating populations of maize with teosinte chromosomal introgressions, an unusual sickly plant phenotype was noted in individuals from crosses with two teosinte accessions collected near Valle de Bravo, Mexico. The plants of these Bravo teosinte accessions appear phenotypically normal themselves and the F plants appear similar to typical maize × teosinte Fs. However, upon backcrossing to maize, the BC and subsequent generations display a number of detrimental characteristics including shorter stature, reduced seed set, and abnormal floral structures. This phenomenon is observed in all BC individuals and there is no chromosomal segment linked to the sickly plant phenotype in advanced backcross generations. Once the sickly phenotype appears in a lineage, normal plants are never again recovered by continued backcrossing to the normal maize parent. Whole-genome shotgun sequencing reveals a small number of genomic sequences, some with homology to transposable elements, that have increased in copy number in the backcross populations. Transcriptome analysis of seedlings, which do not have striking phenotypic abnormalities, identified segments of 18 maize genes that exhibit increased expression in sickly plants. A assembly of transcripts present in plants exhibiting the sickly phenotype identified a set of 59 upregulated novel transcripts. These transcripts include some examples with sequence similarity to transposable elements and other sequences present in the recurrent maize parent (W22) genome as well as novel sequences not present in the W22 genome. Genome-wide profiles of gene expression, DNA methylation, and small RNAs are similar between sickly plants and normal controls, although a few upregulated transcripts and transposable elements are associated with altered small RNA or methylation profiles. This study documents hybrid incompatibility and genome instability triggered by the backcrossing of Bravo teosinte with maize. We name this phenomenon "hybrid decay" and present ideas on the mechanism that may underlie it.
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http://dx.doi.org/10.1534/genetics.119.302378DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727801PMC
September 2019

The genetic architecture of teosinte catalyzed and constrained maize domestication.

Proc Natl Acad Sci U S A 2019 03 6;116(12):5643-5652. Epub 2019 Mar 6.

Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI 53706;

The process of evolution under domestication has been studied using phylogenetics, population genetics-genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance-covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.
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http://dx.doi.org/10.1073/pnas.1820997116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6431195PMC
March 2019

Stepwise cis-Regulatory Changes in ZCN8 Contribute to Maize Flowering-Time Adaptation.

Curr Biol 2018 09 13;28(18):3005-3015.e4. Epub 2018 Sep 13.

National Maize Improvement Center, Key Laboratory of Biology and Genetic Improvement of Maize (MOA), Beijing Key Laboratory of Crop Genetic Improvement, Joint International Research Laboratory of Crop Molecular Breeding, China Agricultural University, Beijing 100193, China. Electronic address:

Maize (Zea mays ssp. mays) was domesticated in southwestern Mexico ∼9,000 years ago from its wild ancestor, teosinte (Zea mays ssp. parviglumis) [1]. From its center of origin, maize experienced a rapid range expansion and spread over 90° of latitude in the Americas [2-4], which required a novel flowering-time adaptation. ZEA CENTRORADIALIS 8 (ZCN8) is the maize florigen gene and has a central role in mediating flowering [5, 6]. Here, we show that ZCN8 underlies a major quantitative trait locus (QTL) (qDTA8) for flowering time that was consistently detected in multiple maize-teosinte experimental populations. Through association analysis in a large diverse panel of maize inbred lines, we identified a SNP (SNP-1245) in the ZCN8 promoter that showed the strongest association with flowering time. SNP-1245 co-segregated with qDTA8 in maize-teosinte mapping populations. We demonstrate that SNP-1245 is associated with differential binding by the flowering activator ZmMADS1. SNP-1245 was a target of selection during early domestication, which drove the pre-existing early flowering allele to near fixation in maize. Interestingly, we detected an independent association block upstream of SNP-1245, wherein the early flowering allele that most likely originated from Zea mays ssp. mexicana introgressed into the early flowering haplotype of SNP-1245 and contributed to maize adaptation to northern high latitudes. Our study demonstrates how independent cis-regulatory variants at a gene can be selected at different evolutionary times for local adaptation, highlighting how complex cis-regulatory control mechanisms evolve. Finally, we propose a polygenic map for the pre-Columbian spread of maize throughout the Americas.
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http://dx.doi.org/10.1016/j.cub.2018.07.029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6537595PMC
September 2018

Construction of the third-generation Zea mays haplotype map.

Gigascience 2018 04;7(4):1-12

Institute of Crop Science, Chinese Academy of Agricultural Sciences/National Key Facilities for Crop Gene Resource and Genetic Improvement, Beijing 100081, China.

Background: Characterization of genetic variations in maize has been challenging, mainly due to deterioration of collinearity between individual genomes in the species. An international consortium of maize research groups combined resources to develop the maize haplotype version 3 (HapMap 3), built from whole-genome sequencing data from 1218 maize lines, covering predomestication and domesticated Zea mays varieties across the world.

Results: A new computational pipeline was set up to process more than 12 trillion bp of sequencing data, and a set of population genetics filters was applied to identify more than 83 million variant sites.

Conclusions: We identified polymorphisms in regions where collinearity is largely preserved in the maize species. However, the fact that the B73 genome used as the reference only represents a fraction of all haplotypes is still an important limiting factor.
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http://dx.doi.org/10.1093/gigascience/gix134DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5890452PMC
April 2018

enhances maize adaptation to higher latitudes.

Proc Natl Acad Sci U S A 2018 01 26;115(2):E334-E341. Epub 2017 Dec 26.

National Maize Improvement Center of China, Beijing Key Laboratory of Crop Genetic Improvement, Laboratory of Crop Heterosis and Utilization, Joint International Research Laboratory of Crop Molecular Breeding, China Agricultural University, Beijing 100193, China;

From its tropical origin in southwestern Mexico, maize spread over a wide latitudinal cline in the Americas. This feat defies the rule that crops are inhibited from spreading easily across latitudes. How the widespread latitudinal adaptation of maize was accomplished is largely unknown. Through positional cloning and association mapping, we resolved a flowering-time quantitative trait locus to a Harbinger-like transposable element positioned 57 kb upstream of a CCT transcription factor (). The Harbinger-like element acts in to repress expression to promote flowering under long days. Knockout of by CRISPR/Cas9 causes early flowering under long days. is diurnally regulated and negatively regulates the expression of the florigen , thereby resulting in late flowering under long days. Population genetics analyses revealed that the Harbinger-like transposon insertion at and the CACTA-like transposon insertion at another CCT paralog, , arose sequentially following domestication and were targeted by selection for maize adaptation to higher latitudes. Our findings help explain how the dynamic maize genome with abundant transposon activity enabled maize to adapt over 90° of latitude during the pre-Columbian era.
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http://dx.doi.org/10.1073/pnas.1718058115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5777075PMC
January 2018

Genome-wide Analysis of Transcriptional Variability in a Large Maize-Teosinte Population.

Mol Plant 2018 03 22;11(3):443-459. Epub 2017 Dec 22.

National Maize Improvement Center of China, Beijing Key Laboratory of Crop Genetic Improvement, Laboratory of Crop Heterosis and Utilization, Joint International Research Laboratory of Crop Molecular Breeding, China Agricultural University, Beijing 100193, China. Electronic address:

Gene expression regulation plays an important role in controlling plant phenotypes and adaptation. Here, we report a comprehensive assessment of gene expression variation through the transcriptome analyses of a large maize-teosinte experimental population. Genome-wide mapping identified 25 660 expression quantitative trait loci (eQTL) for 17 311 genes, capturing an unprecedented range of expression variation. We found that local eQTL were more frequently mapped to adjacent genes, displaying a mode of expression piggybacking, which consequently created co-regulated gene clusters. Genes within the co-regulated gene clusters tend to have relevant functions and shared chromatin modifications. Distant eQTL formed 125 significant distant eQTL hotspots with their targets significantly enriched in specific functional categories. By integrating different sources of information, we identified putative trans- regulators for a variety of metabolic pathways. We demonstrated that the bHLH transcription factor R1 and hexokinase HEX9 might act as crucial regulators for flavonoid biosynthesis and glycolysis, respectively. Moreover, we showed that domestication or improvement has significantly affected global gene expression, with many genes targeted by selection. Of particular interest, the Bx genes for benzoxazinoid biosynthesis may have undergone coordinated cis-regulatory divergence between maize and teosinte, and a transposon insertion that inactivates Bx12 was under strong selection as maize spread into temperate environments with a distinct herbivore community.
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http://dx.doi.org/10.1016/j.molp.2017.12.011DOI Listing
March 2018

Defining the Role of the MADS-Box Gene, Zea Agamous-like1, a Target of Selection During Maize Domestication.

J Hered 2018 03;109(3):333-338

Laboratory of Genetics, The University of Wisconsin-Madison, Madison, WI.

Genomic scans for genes that show the signature of past selection have been widely applied to a number of species and have identified a large number of selection candidate genes. In cultivated maize (Zea mays ssp. mays) selection scans have identified several hundred candidate domestication genes by comparing nucleotide diversity and differentiation between maize and its progenitor, teosinte (Z. mays ssp. parviglumis). One of these is a gene called zea agamous-like1 (zagl1), a MADS-box transcription factor, that is known for its function in the control of flowering time. To determine the trait(s) controlled by zagl1 that was (were) the target(s) of selection during maize domestication, we created a set of recombinant chromosome isogenic lines that differ for the maize versus teosinte alleles of zagl1 and which carry cross-overs between zagl1 and its neighbor genes. These lines were grown in a randomized trial and scored for flowering time and domestication related traits. The results indicated that the maize versus teosinte alleles of zagl1 affect flowering time as expected, as well as multiple traits related to ear size with the maize allele conferring larger ears with more kernels. Our results suggest that zagl1 may have been under selection during domestication to increase the size of the maize ear.
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http://dx.doi.org/10.1093/jhered/esx073DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7189973PMC
March 2018

Selection During Maize Domestication Targeted a Gene Network Controlling Plant and Inflorescence Architecture.

Genetics 2017 10 28;207(2):755-765. Epub 2017 Jul 28.

Laboratory of Genetics, University of Wisconsin-Madison, Wisconsin 53076

Selection during evolution, whether natural or artificial, acts through the phenotype. For multifaceted phenotypes such as plant and inflorescence architecture, the underlying genetic architecture is comprised of a complex network of interacting genes rather than single genes that act independently to determine the trait. As such, selection acts on entire gene networks. Here, we begin to define the genetic regulatory network to which the maize domestication gene, (), belongs. Using a combination of molecular methods to uncover either direct or indirect regulatory interactions, we identified a set of genes that lie downstream of in a gene network regulating both plant and inflorescence architecture. Additional genes, known from the literature, also act in this network. We observed that regulates both core cell cycle genes and another maize domestication gene, (). We show that several members of the MADS-box gene family are either directly or indirectly regulated by and/or , and that sits atop a cascade of transcriptional regulators controlling both plant and inflorescence architecture. Multiple members of the network appear to have been the targets of selection during maize domestication. Knowledge of the regulatory hierarchies controlling traits is central to understanding how new morphologies evolve.
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http://dx.doi.org/10.1534/genetics.117.300071DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5629337PMC
October 2017

A Gene for Genetic Background in Zea mays: Fine-Mapping enhancer of teosinte branched1.2 to a YABBY Class Transcription Factor.

Genetics 2016 Dec 11;204(4):1573-1585. Epub 2016 Oct 11.

Laboratory of Genetics, University of Wisconsin-Madison, Wisconsin 53706

The effects of an allelic substitution at a gene often depend critically on genetic background, i.e., the genotypes at other genes in the genome. During the domestication of maize from its wild ancestor (teosinte), an allelic substitution at teosinte branched (tb1) caused changes in both plant and ear architecture. The effects of tb1 on phenotype were shown to depend on multiple background loci, including one called enhancer of tb1.2 (etb1.2). We mapped etb1.2 to a YABBY class transcription factor (ZmYAB2.1) and showed that the maize alleles of ZmYAB2.1 are either expressed at a lower level than teosinte alleles or disrupted by insertions in the sequences. tb1 and etb1.2 interact epistatically to control the length of internodes within the maize ear, which affects how densely the kernels are packed on the ear. The interaction effect is also observed at the level of gene expression, with tb1 acting as a repressor of ZmYAB2.1 expression. Curiously, ZmYAB2.1 was previously identified as a candidate gene for another domestication trait in maize, nonshattering ears. Consistent with this proposed role, ZmYAB2.1 is expressed in a narrow band of cells in immature ears that appears to represent a vestigial abscission (shattering) zone. Expression in this band of cells may also underlie the effect on internode elongation. The identification of ZmYAB2.1 as a background factor interacting with tb1 is a first step toward a gene-level understanding of how tb1 and the background within which it works evolved in concert during maize domestication.
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http://dx.doi.org/10.1534/genetics.116.194928DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5161286PMC
December 2016

Mapping Prolificacy QTL in Maize and Teosinte.

J Hered 2016 22;107(7):674-678. Epub 2016 Sep 22.

From the Life Science College, Shanxi Normal University, No. 1 Gongyuan Street, Linfen City, Shanxi Province 041004, China (L. Yang) and Laboratory of Genetics, University of Wisconsin-Madison, 425 Henry Mall, Madison, WI 53706 (C. J. Yang, Cheng, Xue, and Doebley).

Teosinte, the ancestor of maize, possesses multiple ears at each node along its main stalk, whereas maize has only a single ear at each node. With its greater ear number, teosinte is referred to as being more prolific. The grassy tillers 1 (gt1) gene has been identified as a large-effect quantitative trait locus underlying this prolificacy difference between maize and teosinte, and the causal polymorphism for the difference was mapped to a 2.7kb control region 5' of the gt1 ORF. The most common maize haplotype (M1) at the gt1 control region confers low prolificacy. A prior study reported that 29% of maize varieties possess the teosinte haplotype (T) for the control region, although these varieties are nonprolific. This observation suggested that these maize lines might possess an additional factor, other than gt1, suppressing prolificacy in maize. We discovered that the factor suppressing prolificacy in maize varieties with the gt1 T haplotype mapped to a 3.20 cM interval, which includes gt1 Subsequent DNA sequence analysis revealed that the maize varieties with the apparent T haplotype actually possess a distinct maize haplotype (M2) that is similar, but not identical, to the T haplotype in sequence but is associated with a nonprolific phenotype similar to the M1 haplotype. Our data indicate that the M2 haplotype or a closely linked factor confers a nonprolific phenotype. Our data suggest that 2 different alleles or haplotypes (M1 and M2) of gt1 were selected during domestication, and that nonprolificacy in all maize varieties is likely a result of allele substitutions at gt1.
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http://dx.doi.org/10.1093/jhered/esw064DOI Listing
July 2017

Fine Mapping of a QTL Associated with Kernel Row Number on Chromosome 1 of Maize.

PLoS One 2016 1;11(3):e0150276. Epub 2016 Mar 1.

Laboratory of Genetics, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

The genetic factors underlying changes in ear morphology, and particularly the inheritance of kernel row number (KRN), have been broadly investigated in diverse mapping populations in maize (Zea mays L.). In this study, we mapped a region on the long arm of chromosome 1 containing a QTL for KRN. This work was performed using a set of recombinant chromosome nearly isogenic lines (RCNILs) derived from a BC2S3 population produced using the inbred maize line W22 and teosinte (Zea mays ssp. parviglumis) as the parents. A set of 48 RCNILs was evaluated in the field during the summer of 2013 in order to perform the mapping. A QTL for KRN was found that explained approximately 51% of the phenotypic variance and had a 1.5-LOD confidence interval of 203 kb. Seven genes are described in this interval. One of these candidate genes may have been the target of domestication processes in maize and contributed to the shift from two kernel row ears in teosinte to a highly polystichous ear in maize.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0150276PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4773258PMC
July 2016

Evidence That the Origin of Naked Kernels During Maize Domestication Was Caused by a Single Amino Acid Substitution in tga1.

Genetics 2015 Jul 4;200(3):965-74. Epub 2015 May 4.

Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin 53076

teosinte glume architecture1 (tga1), a member of the SBP-box gene family of transcriptional regulators, has been identified as the gene conferring naked kernels in maize vs. encased kernels in its wild progenitor, teosinte. However, the identity of the causative polymorphism within tga1 that produces these different phenotypes has remained unknown. Using nucleotide diversity data, we show that there is a single fixed nucleotide difference between maize and teosinte in tga1, and this difference confers a Lys (teosinte allele) to Asn (maize allele) substitution. This substitution transforms TGA1 into a transcriptional repressor. While both alleles of TGA1 can bind a GTAC motif, maize-TGA1 forms more stable dimers than teosinte-TGA1. Since it is the only fixed difference between maize and teosinte, this alteration in protein function likely underlies the differences in maize and teosinte glume architecture. We previously reported a difference in TGA1 protein abundance between maize and teosinte based on relative signal intensity of a Western blot. Here, we show that this signal difference is not due to tga1 but to a second gene, neighbor of tga1 (not1). Not1 encodes a protein that has 92% amino acid similarity to TGA1 and that is recognized by the TGA1 antibody. Genetic mapping and phenotypic data show that tga1, without a contribution from not1, controls the difference in covered vs. naked kernels. No trait differences could be associated with the maize vs. teosinte alleles of not1. Our results document how morphological evolution can be driven by a simple nucleotide change that alters protein function.
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http://dx.doi.org/10.1534/genetics.115.175752DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4512555PMC
July 2015

The role of cis regulatory evolution in maize domestication.

PLoS Genet 2014 Nov 6;10(11):e1004745. Epub 2014 Nov 6.

Laboratory of Genetics, University of Wisconsin - Madison, Madison, Wisconsin, United States of America.

Gene expression differences between divergent lineages caused by modification of cis regulatory elements are thought to be important in evolution. We assayed genome-wide cis and trans regulatory differences between maize and its wild progenitor, teosinte, using deep RNA sequencing in F1 hybrid and parent inbred lines for three tissue types (ear, leaf and stem). Pervasive regulatory variation was observed with approximately 70% of ∼17,000 genes showing evidence of regulatory divergence between maize and teosinte. However, many fewer genes (1,079 genes) show consistent cis differences with all sampled maize and teosinte lines. For ∼70% of these 1,079 genes, the cis differences are specific to a single tissue. The number of genes with cis regulatory differences is greatest for ear tissue, which underwent a drastic transformation in form during domestication. As expected from the domestication bottleneck, maize possesses less cis regulatory variation than teosinte with this deficit greatest for genes showing maize-teosinte cis regulatory divergence, suggesting selection on cis regulatory differences during domestication. Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not. We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression. Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.
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http://dx.doi.org/10.1371/journal.pgen.1004745DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4222645PMC
November 2014

Genetic dissection of a genomic region with pleiotropic effects on domestication traits in maize reveals multiple linked QTL.

Genetics 2014 Sep 20;198(1):345-53. Epub 2014 Jun 20.

Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin 53706.

The domesticated crop maize and its wild progenitor, teosinte, have been used in numerous experiments to investigate the nature of divergent morphologies. This study examines a poorly understood region on the fifth chromosome of maize associated with a number of traits under selection during domestication, using a quantitative trait locus (QTL) mapping population specific to the fifth chromosome. In contrast with other major domestication loci in maize where large-effect, highly pleiotropic, single genes are responsible for phenotypic effects, our study found the region on chromosome five fractionates into multiple-QTL regions, none with singularly large effects. The smallest 1.5-LOD support interval for a QTL contained 54 genes, one of which was a MADS MIKC(C) transcription factor, a family of proteins implicated in many developmental programs. We also used simulated trait data sets to investigate the power of our mapping population to identify QTL for which there is a single underlying causal gene. This analysis showed that while QTL for traits controlled by single genes can be accurately mapped, our population design can detect no more than ∼4.5 QTL per trait even when there are 100 causal genes. Thus when a trait is controlled by ≥5 genes in the simulated data, the number of detected QTL can represent a simplification of the underlying causative factors. Our results show how a QTL region with effects on several domestication traits may be due to multiple linked QTL of small effect as opposed to a single gene with large and pleiotropic effects.
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http://dx.doi.org/10.1534/genetics.114.165845DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4174946PMC
September 2014

Defining the Role of prolamin-box binding factor1 Gene During Maize Domestication.

J Hered 2014 Jul-Aug;105(4):576-582. Epub 2014 Mar 28.

From the Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, No.12 Zhongguancun Nandajie, Beijing 100081, China (Lang); the Department of Genetics, University of Wisconsin-Madison, 425 Henry Mall, Madison, WI 53706 (Wills, Lemmon, Shannon, and Doebley); the Department of Biomedical Sciences, Cornell University, T8 016D Veterinary Research Tower, Ithaca, NY 14853 (Shannon); the Computational Biology Service Unit, Cornell University, 620 Rhodes Hall, Ithaca, NY 14853 (Bukowski); Waksman Institute of Microbiology, Rutgers University, 190 Frelinghuysen Road, Piscataway, NJ 08854 (Wu and Messing); and the Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, CAS, 300 Feng Lin Road, Shanghai 200032, China (Wu).

The prolamin-box binding factor1 (pbf1) gene encodes a transcription factor that controls the expression of seed storage protein (zein) genes in maize. Prior studies show that pbf1 underwent selection during maize domestication although how it affected trait change during domestication is unknown. To assay how pbf1 affects phenotypic differences between maize and teosinte, we compared nearly isogenic lines (NILs) that differ for a maize versus teosinte allele of pbf1 Kernel weight for the teosinte NIL (162mg) is slightly but significantly greater than that for the maize NIL (156mg). RNAseq data for developing kernels show that the teosinte allele of pbf1 is expressed at about twice the level of the maize allele. However, RNA and protein assays showed no difference in zein profile between the two NILs. The lower expression for the maize pbf1 allele suggests that selection may have favored this change; however, how reduced pbf1 expression alters phenotype remains unknown. One possibility is that pbf1 regulates genes other than zeins and thereby is a domestication trait. The observed drop in seed weight associated with the maize allele of pbf1 is counterintuitive but could represent a negative pleiotropic effect of selection on some other aspect of kernel composition.
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http://dx.doi.org/10.1093/jhered/esu019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6373496PMC
September 2017

From many, one: genetic control of prolificacy during maize domestication.

PLoS Genet 2013 Jun 27;9(6):e1003604. Epub 2013 Jun 27.

Department of Genetics, University of Wisconsin-Madison, Madison, WI, USA.

A reduction in number and an increase in size of inflorescences is a common aspect of plant domestication. When maize was domesticated from teosinte, the number and arrangement of ears changed dramatically. Teosinte has long lateral branches that bear multiple small ears at their nodes and tassels at their tips. Maize has much shorter lateral branches that are tipped by a single large ear with no additional ears at the branch nodes. To investigate the genetic basis of this difference in prolificacy (the number of ears on a plant), we performed a genome-wide QTL scan. A large effect QTL for prolificacy (prol1.1) was detected on the short arm of chromosome 1 in a location that has previously been shown to influence multiple domestication traits. We fine-mapped prol1.1 to a 2.7 kb "causative region" upstream of the grassy tillers1 (gt1) gene, which encodes a homeodomain leucine zipper transcription factor. Tissue in situ hybridizations reveal that the maize allele of prol1.1 is associated with up-regulation of gt1 expression in the nodal plexus. Given that maize does not initiate secondary ear buds, the expression of gt1 in the nodal plexus in maize may suppress their initiation. Population genetic analyses indicate positive selection on the maize allele of prol1.1, causing a partial sweep that fixed the maize allele throughout most of domesticated maize. This work shows how a subtle cis-regulatory change in tissue specific gene expression altered plant architecture in a way that improved the harvestability of maize.
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http://dx.doi.org/10.1371/journal.pgen.1003604DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3694832PMC
June 2013

ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize.

Proc Natl Acad Sci U S A 2012 Jul 18;109(28):E1913-21. Epub 2012 Jun 18.

Department of Crop Science, North Carolina State University, Raleigh, NC 27695, USA.

Teosinte, the progenitor of maize, is restricted to tropical environments in Mexico and Central America. The pre-Columbian spread of maize from its center of origin in tropical Southern Mexico to the higher latitudes of the Americas required postdomestication selection for adaptation to longer day lengths. Flowering time of teosinte and tropical maize is delayed under long day lengths, whereas temperate maize evolved a reduced sensitivity to photoperiod. We measured flowering time of the maize nested association and diverse association mapping panels in the field under both short and long day lengths, and of a maize-teosinte mapping population under long day lengths. Flowering time in maize is a complex trait affected by many genes and the environment. Photoperiod response is one component of flowering time involving a subset of flowering time genes whose effects are strongly influenced by day length. Genome-wide association and targeted high-resolution linkage mapping identified ZmCCT, a homologue of the rice photoperiod response regulator Ghd7, as the most important gene affecting photoperiod response in maize. Under long day lengths ZmCCT alleles from diverse teosintes are consistently expressed at higher levels and confer later flowering than temperate maize alleles. Many maize inbred lines, including some adapted to tropical regions, carry ZmCCT alleles with no sensitivity to day length. Indigenous farmers of the Americas were remarkably successful at selecting on genetic variation at key genes affecting the photoperiod response to create maize varieties adapted to vastly diverse environments despite the hindrance of the geographic axis of the Americas and the complex genetic control of flowering time.
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http://dx.doi.org/10.1073/pnas.1203189109DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3396540PMC
July 2012

Evidence for a natural allelic series at the maize domestication locus teosinte branched1.

Genetics 2012 Jul 13;191(3):951-8. Epub 2012 Apr 13.

Department of Genetics, University of Wisconsin, Madison, WI 53706, USA.

Despite numerous quantitative trait loci and association mapping studies, our understanding of the extent to which natural allelic series contribute to the variation for complex traits is limited. In this study, we investigate the occurrence of a natural allelic series for complex traits at the teosinte branched1 (tb1) gene in natural populations of teosinte (Zea mays ssp. parviglumis, Z. mays ssp. mexicana, and Z. diploperennis). Previously, tb1 was shown to confer large effects on both plant architecture and ear morphology between domesticated maize and teosinte; however, the effect of tb1 on trait variation in natural populations of teosinte has not been investigated. We compare the effects of nine teosinte alleles of tb1 that were introgressed into an isogenic maize inbred background. Our results provide evidence for a natural allelic series at tb1 for several complex morphological traits. The teosinte introgressions separate into three distinct phenotypic classes, which correspond to the taxonomic origin of the alleles. The effects of the three allelic classes also correspond to known morphological differences between the teosinte taxa. Our results suggest that tb1 contributed to the morphological diversification of teosinte taxa as well as to the domestication of maize.
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http://dx.doi.org/10.1534/genetics.112.138479DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3389986PMC
July 2012

Do large effect QTL fractionate? A case study at the maize domestication QTL teosinte branched1.

Genetics 2011 Jul 21;188(3):673-81. Epub 2011 Apr 21.

Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706, USA.

Quantitative trait loci (QTL) mapping is a valuable tool for studying the genetic architecture of trait variation. Despite the large number of QTL studies reported in the literature, the identified QTL are rarely mapped to the underlying genes and it is usually unclear whether a QTL corresponds to one or multiple linked genes. Similarly, when QTL for several traits colocalize, it is usually unclear whether this is due to the pleiotropic action of a single gene or multiple linked genes, each affecting one trait. The domestication gene teosinte branched1 (tb1) was previously identified as a major domestication QTL with large effects on the differences in plant and ear architecture between maize and teosinte. Here we present the results of two experiments that were performed to determine whether the single gene tb1 explains all trait variation for its genomic region or whether the domestication QTL at tb1 fractionates into multiple linked QTL. For traits measuring plant architecture, we detected only one QTL per trait and these QTL all mapped to tb1. These results indicate that tb1 is the sole gene for plant architecture traits that segregates in our QTL mapping populations. For most traits related to ear morphology, we detected multiple QTL per trait in the tb1 genomic region, including a large effect QTL at tb1 itself plus one or two additional linked QTL. tb1 is epistatic to two of these additional QTL for ear traits. Overall, these results provide examples for both a major QTL that maps to a single gene, as well as a case in which a QTL fractionates into multiple linked QTL.
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http://dx.doi.org/10.1534/genetics.111.126508DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3176526PMC
July 2011

Using association mapping in teosinte to investigate the function of maize selection-candidate genes.

PLoS One 2009 Dec 9;4(12):e8227. Epub 2009 Dec 9.

Laboratory of Genetics, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

Background: Large-scale screens of the maize genome identified 48 genes that show the putative signature of artificial selection during maize domestication or improvement. These selection-candidate genes may act as quantitative trait loci (QTL) that control the phenotypic differences between maize and its progenitor, teosinte. The selection-candidate genes appear to be located closer in the genome to domestication QTL than expected by chance.

Methods And Findings: As a step toward defining the traits controlled by these genes, we performed phenotype-genotype association mapping in teosinte for 32 of the 48 plus three other selection-candidate genes. Our analyses assayed 32 phenotypic traits, many of which were altered during maize domestication or improvement. We observed several significant associations between SNPs in the selection-candidate genes and trait variation in teosinte. These included two associations that surpassed the Bonferroni correction and five instances where a gene significantly associated with the same trait in both of our association mapping panels. Despite these significant associations, when compared as a group the selection-candidate genes performed no better than randomly chosen genes.

Conclusions: Our results suggest association analyses can be helpful for identifying traits under the control of selection-candidate genes. Indeed, we present evidence for new functions for several selection-candidate genes. However, with the current set of selection-candidate genes and our association mapping strategy, we found very few significant associations overall and no more than we would have found with randomly chosen genes. We discuss possible reasons that a large number of significant genotype-phenotype associations were not discovered.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0008227PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2785427PMC
December 2009

The molecular genetics of crop domestication.

Cell 2006 Dec;127(7):1309-21

Department of Genetics, University of Wisconsin, Madison, WI 53706, USA.

Ten thousand years ago human societies around the globe began to transition from hunting and gathering to agriculture. By 4000 years ago, ancient peoples had completed the domestication of all major crop species upon which human survival is dependent, including rice, wheat, and maize. Recent research has begun to reveal the genes responsible for this agricultural revolution. The list of genes to date tentatively suggests that diverse plant developmental pathways were the targets of Neolithic "genetic tinkering," and we are now closer to understanding how plant development was redirected to meet the needs of a hungry world.
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http://dx.doi.org/10.1016/j.cell.2006.12.006DOI Listing
December 2006

A unified mixed-model method for association mapping that accounts for multiple levels of relatedness.

Nat Genet 2006 Feb 25;38(2):203-8. Epub 2005 Dec 25.

Institute for Genomic Diversity, Cornell University, Ithaca, New York 14853, USA.

As population structure can result in spurious associations, it has constrained the use of association studies in human and plant genetics. Association mapping, however, holds great promise if true signals of functional association can be separated from the vast number of false signals generated by population structure. We have developed a unified mixed-model approach to account for multiple levels of relatedness simultaneously as detected by random genetic markers. We applied this new approach to two samples: a family-based sample of 14 human families, for quantitative gene expression dissection, and a sample of 277 diverse maize inbred lines with complex familial relationships and population structure, for quantitative trait dissection. Our method demonstrates improved control of both type I and type II error rates over other methods. As this new method crosses the boundary between family-based and structured association samples, it provides a powerful complement to currently available methods for association mapping.
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http://dx.doi.org/10.1038/ng1702DOI Listing
February 2006

A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement.

Plant Cell 2005 Nov 14;17(11):2859-72. Epub 2005 Oct 14.

Division of Plant Sciences, University of Missouri, Columbia, Misssouri 65211, USA.

Maize (Zea mays subsp mays) was domesticated from teosinte (Z. mays subsp parviglumis) through a single domestication event in southern Mexico between 6000 and 9000 years ago. This domestication event resulted in the original maize landrace varieties, which were spread throughout the Americas by Native Americans and adapted to a wide range of environmental conditions. Starting with landraces, 20th century plant breeders selected inbred lines of maize for use in hybrid maize production. Both domestication and crop improvement involved selection of specific alleles at genes controlling key morphological and agronomic traits, resulting in reduced genetic diversity relative to unselected genes. Here, we sequenced 1095 maize genes from a sample of 14 inbred lines and chose 35 genes with zero sequence diversity as potential targets of selection. These 35 genes were then sequenced in a sample of diverse maize landraces and teosintes and tested for selection. Using two statistical tests, we identified eight candidate genes. Extended gene sequencing of these eight candidate loci confirmed that six were selected throughout the gene, and the remaining two exhibited evidence of selection in the 3' portion of each gene. The selected genes have functions consistent with agronomic selection for nutritional quality, maturity, and productivity. Our large-scale screen for artificial selection allows identification of genes of potential agronomic importance even when gene function and the phenotype of interest are unknown.
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http://dx.doi.org/10.1105/tpc.105.037242DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1276015PMC
November 2005

Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication.

Genetics 2006 Jan 3;172(1):519-31. Epub 2005 Oct 3.

Department of Genetics, University of Wisconsin, Madison, Wisconsin, 53706, USA.

Phenotypic variation on which selection can act during evolution may be caused by variation in activity level of developmental regulatory genes. In many cases, however, such genes affect multiple traits. This situation can lead to co-evolution of traits, or evolutionary constraint if some pleiotropic effects are detrimental. Here, we present an analysis of quantitative traits associated with gene copy number of two important maize regulatory genes, the duplicate FLORICAULA/LEAFY orthologs zfl1 and zfl2. We found statistically significant associations between several quantitative traits and copy number of both zfl genes in several maize genetic backgrounds. Despite overlap in traits associated with these duplicate genes, zfl1 showed stronger associations with flowering time, while zfl2 associated more strongly with branching and inflorescence structure traits, suggesting some divergence of function. Since zfl2 associates with quantitative variation for ear rank and also maps near a quantitative trait locus (QTL) on chromosome 2 controlling ear rank differences between maize and teosinte, we tested whether zfl2 might have been involved in the evolution of this trait using a QTL complementation test. The results suggest that zfl2 activity is important for the QTL effect, supporting zfl2 as a candidate gene for a role in morphological evolution of maize.
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http://dx.doi.org/10.1534/genetics.105.048595DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1456179PMC
January 2006

The origin of the naked grains of maize.

Nature 2005 Aug;436(7051):714-9

Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin 53706, USA.

The most critical step in maize (Zea mays ssp. mays) domestication was the liberation of the kernel from the hardened, protective casing that envelops the kernel in the maize progenitor, teosinte. This evolutionary step exposed the kernel on the surface of the ear, such that it could readily be used by humans as a food source. Here we show that this key event in maize domestication is controlled by a single gene (teosinte glume architecture or tga1), belonging to the SBP-domain family of transcriptional regulators. The factor controlling the phenotypic difference between maize and teosinte maps to a 1-kilobase region, within which maize and teosinte show only seven fixed differences in their DNA sequences. One of these differences encodes a non-conservative amino acid substitution and may affect protein function, and the other six differences potentially affect gene regulation. Molecular evolution analyses show that this region was the target of selection during maize domestication. Our results demonstrate that modest genetic changes in single genes can induce dramatic changes in phenotype during domestication and evolution.
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http://dx.doi.org/10.1038/nature03863DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1464477PMC
August 2005

The effects of artificial selection on the maize genome.

Science 2005 May;308(5726):1310-4

Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA.

Domestication promotes rapid phenotypic evolution through artificial selection. We investigated the genetic history by which the wild grass teosinte (Zea mays ssp. parviglumis) was domesticated into modern maize (Z. mays ssp. mays). Analysis of single-nucleotide polymorphisms in 774 genes indicates that 2 to 4% of these genes experienced artificial selection. The remaining genes retain evidence of a population bottleneck associated with domestication. Candidate selected genes with putative function in plant growth are clustered near quantitative trait loci that contribute to phenotypic differences between maize and teosinte. If we assume that our sample of genes is representative, approximately 1200 genes throughout the maize genome have been affected by artificial selection.
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http://dx.doi.org/10.1126/science.1107891DOI Listing
May 2005

Molecular evolution of FLORICAULA/LEAFY orthologs in the Andropogoneae (Poaceae).

Mol Biol Evol 2005 Apr 2;22(4):1082-94. Epub 2005 Feb 2.

Department of Genetics, University of Wisconsin-Madison, USA.

Members of the grass family (Poaceae) exhibit a broad range of inflorescence structures and other morphologies, making the grasses an interesting model system for studying the evolution of development. Here we present an analysis of the molecular evolution of FLORICAULA/LEAFY-like genes, which are important developmental regulatory loci known to affect inflorescence development in a wide range of flowering plant species. We have focused on sequences from the Andropogoneae, a tribe within the grass family that includes maize (Zea mays ssp. mays) and Sorghum (Sorghum bicolor). The FLORICAULA/LEAFY gene phylogeny we generated largely agrees with previously published phylogenies for the Andropogoneae using other nuclear genes but is unique in that it includes both members of one of the many duplicate gene sets present in maize. The placement of these sequences in the phylogeny suggests that the duplication of the maize FLORICAULA/LEAFY orthologs, zfl1 and zfl2, is a consequence of a proposed tetraploidy event that occurred in the common ancestor of Zea and a closely related genus, Tripsacum. Our data are consistent with the hypothesis that the transcribed regions of the FLORICAULA/LEAFY-like genes in the Andropogoneae are functionally constrained at both nonsynonymous and synonymous sites and show no evidence of directional selection. We also examined conservation of short noncoding sequences in the first intron, which may play a role in gene regulation. Finally, we investigated the genetic diversity of one of the two maize FLORICAULA/LEAFY orthologs, zfl2, in maize and its wild ancestor, teosinte (Z. mays ssp. parviglumis), and found no evidence for selection pressure resulting from maize domestication within the zfl2-coding region.
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http://dx.doi.org/10.1093/molbev/msi095DOI Listing
April 2005
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