Title: Selection Signatures Underlying Dramatic Male Inflorescence Transformation During Modern Hybrid Maize Breeding

Journal Article · · Genetics (Online)

Inflorescence capacity plays a crucial role in reproductive fitness in plants, and in production of hybrid crops. Maize is a monoecious species bearing separate male and female flowers (tassel and ear, respectively). The switch from open-pollinated populations of maize to hybrid-based breeding schemes in the early 20th century was accompanied by a dramatic reduction in tassel size, and the trend has continued with modern breeding over the recent decades. The goal of this study was to identify selection signatures in genes that may underlie this dramatic transformation. Using a population of 942 diverse inbred maize accessions and a nested association mapping population comprising three 200-line biparental populations, we measured 15 tassel morphological characteristics by manual and image-based methods. Genome-wide association studies identified 242 single nucleotide polymorphisms significantly associated with measured traits. We compared 41 unselected lines from the Iowa Stiff Stalk Synthetic (BSSS) population to 21 highly selected lines developed by modern commercial breeding programs, and found that tassel size and weight were reduced significantly. We assayed genetic differences between the two groups using three selection statistics: cross population extended haplotype homozogysity, cross-population composite likelihood ratio, and fixation index. All three statistics show evidence of selection at genomic regions associated with tassel morphology relative to genome-wide null distributions. These results support the tremendous effect, both phenotypic and genotypic, that selection has had on maize male inflorescence morphology.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231; FC02-07ER64494
OSTI ID:
1609250
Journal Information:
Genetics (Online), Journal Name: Genetics (Online) Journal Issue: 3 Vol. 210; ISSN 1943-2631
Publisher:
Oxford University Press; Genetics Society of AmericaCopyright Statement
Country of Publication:
United States
Language:
English

References (70)

The origin of the naked grains of maize journal August 2005
Genome-wide genetic association of complex traits in heterogeneous stock mice journal July 2006
Genetic similarity among European winter triticale elite germplasms assessed with AFLP and comparisons with SSR and pedigree data journal April 2005
Exploring evidence of positive selection reveals genetic basis of meat quality traits in Berkshire pigs through whole genome sequencing journal August 2015
barren inflorescence2 regulates axillary meristem development in the maize inflorescence journal August 2001
Correction: A Map of Recent Positive Selection in the Human Genome journal June 2007
The pls Package: Principal Component and Partial Least Squares Regression in R journal January 2007
Effect of Tassel Removal on Grain Yield of Corn (Zea mays L.)1 journal January 1969
Data from: Selection signatures underlying dramatic male inflorescence transformation during modern hybrid maize breeding dataset January 2018
Genetic and QTL analysis of maize tassel and ear inflorescence architecture journal January 2006
Frequency of the transposable element Uq in Iowa stiff stalk synthetic maize populations journal February 1991
The origin of the naked grains of maize journal August 2005
Genome-wide detection and characterization of positive selection in human populations journal October 2007
Whole-genome resequencing reveals loci under selection during chicken domestication journal March 2010
Improved maize reference genome with single-molecule technologies journal June 2017
Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean journal February 2015
Comparative population genomics of maize domestication and improvement journal June 2012
Genome-wide association study of leaf architecture in the maize nested association mapping population journal January 2011
Genome-wide genetic association of complex traits in heterogeneous stock mice journal July 2006
Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation journal December 2014
Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection journal September 2015
A Fast and Flexible Statistical Model for Large-Scale Population Genotype Data: Applications to Inferring Missing Genotypes and Haplotypic Phase journal April 2006
Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants journal February 2009
TASSEL: software for association mapping of complex traits in diverse samples journal June 2007
teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. journal September 1995
hapbin: An Efficient Program for Performing Haplotype-Based Scans for Positive Selection in Large Genomic Datasets: Fig. 1. journal August 2015
Fast model-based estimation of ancestry in unrelated individuals journal July 2009
Population differentiation as a test for selective sweeps journal January 2010
Insights into the Maize Pan-Genome and Pan-Transcriptome journal January 2014
Maize association population: a high-resolution platform for quantitative trait locus dissection journal November 2005
Tansley Review No. 27 The control of carbon partitioning in plants journal November 1990
ESTIMATING F -STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE journal November 1984
Fifteen years of genomewide scans for selection: trends, lessons and unaddressed genetic sources of complication journal September 2015
Complex genetic architecture underlies maize tassel domestication journal January 2017
Joint-linkage mapping and GWAS reveal extensive genetic loci that regulate male inflorescence size in maize journal January 2016
The limited role of differential fractionation in genome content variation and function in maize ( Zea mays L .) inbred lines journal December 2017
The Genetic Architecture of Maize Flowering Time journal August 2009
Genetic Properties of the Maize Nested Association Mapping Population journal August 2009
A genome-wide scan for signatures of selection in Chinese indigenous and commercial pig breeds journal January 2014
A genome-wide scan for signatures of differential artificial selection in ten cattle breeds journal January 2013
Exploring evidence of positive selection reveals genetic basis of meat quality traits in Berkshire pigs through whole genome sequencing journal August 2015
TIPS: a system for automated image-based phenotyping of maize tassels journal March 2017
Second-generation PLINK: rising to the challenge of larger and richer datasets journal February 2015
Table for Estimating the Goodness of Fit of Empirical Distributions journal June 1948
barren inflorescence2 regulates axillary meristem development in the maize inflorescence journal August 2001
A Time Petri Net Extended with Price Information journal January 2007
A Map of Recent Positive Selection in the Human Genome journal March 2006
Distinct Genetic Architectures for Male and Female Inflorescence Traits of Maize journal November 2011
Association Mapping across Numerous Traits Reveals Patterns of Functional Variation in Maize journal December 2014
Iterative Usage of Fixed and Random Effect Models for Powerful and Efficient Genome-Wide Association Studies journal February 2016
A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species journal May 2011
Pleiotropic Effects of the Duplicate Maize FLORICAULA/LEAFY Genes zfl1 and zfl2 on Traits Under Selection During Maize Domestication journal October 2005
A Genome-Wide Scan for Evidence of Selection in a Maize Population Under Long-Term Artificial Selection for Ear Number journal December 2013
The pls Package: Principal Component and Partial Least Squares Regression in R journal January 2007
Fitting Linear Mixed-Effects Models Using lme4 journal January 2015
Tassels and the Productivity of Maize1 journal January 1967
Effect of Tassel Removal on Grain Yield of Corn (Zea mays L.)1 journal January 1969
Inbreeding Depression, Inbred and Hybrid Grain Yields, and Other Traits of Maize Genotypes Representing Three Eras1 journal January 1984
Recurrent Selection for Reduced Tassel Branch Number and Reduced Leaf Area Density above the Ear in Tropical Maize Populations 1 journal November 1987
Quantitative Trait Loci for Tassel Traits in Maize journal January 1999
Quantitative Trait Loci Controlling Leaf and Tassel Traits in a B73 × Mo17 Population of Maize journal January 2002
Evolution of North American Dent Corn from Public to Proprietary Germplasm journal May 2006
Can Changes in Canopy and/or Root System Architecture Explain Historical Maize Yield Trends in the U.S. Corn Belt? journal January 2009
Changes in Plant Morphology in Response to Recurrent Selection in the Iowa Stiff Stalk Synthetic Maize Population journal November 2011
Comparing Individual Means in the Analysis of Variance journal June 1949
Novel Methods to Optimize Genotypic Imputation for Low-Coverage, Next-Generation Sequence Data in Crop Plants journal January 2014
Data from: Selection signatures underlying dramatic male inflorescence transformation during modern hybrid maize breeding dataset January 2018
Data from: Genome-wide association analysis of stalk biomass and anatomical traits in maize dataset January 2019
Exploring evidence of positive selection reveals genetic basis of meat quality traits in Berkshire pigs through whole genome sequencing collection January 2015
TIPS: a system for automated image-based phenotyping of maize tassels dataset March 2017

Cited By (3)