Peter L. Morrell

Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars

Domesticated crops experience strong human-mediated selection aimed at developing high-yielding varieties adapted to local conditions. To detect regions of the wheat genome subject to selection during improvement, we developed a high-throughput array to interrogate 9,000 gene-associated single-nucleotide polymorphisms (SNP) in a worldwide sample of 2,994 accessions of hexaploid wheat including landraces and modern cultivars. Using a SNP-based diversity map we characterized the impact of crop improvement on genomic and geographic patterns of genetic diversity. We found evidence of a small population bottleneck and extensive use of ancestral variation often traceable to founders of cultivars from diverse geographic regions. Analyzing genetic differentiation among populations and the extent of haplotype sharing, we identified allelic variants subjected to selection during improvement. Selective sweeps were found around genes involved in the regulation of flowering time and phenology. An introgression of a wild relative-derived gene conferring resistance to a fungal pathogen was detected by haplotype-based analysis. Comparing selective sweeps identified in different populations, we show that selection likely acts on distinct targets or multiple functionally equivalent alleles in different portions of the geographic range of wheat. The majority of the selected alleles were present at low frequency in local populations, suggesting either weak selection pressure or temporal variation in the targets of directional selection during breeding probably associated with changing agricultural practices or environmental conditions. The developed SNP chip and map of genetic variation provide a resource for advancing wheat breeding and supporting future population genomic and genome-wide association studies in wheat.

Comparative population genomics of maize domestication and improvement

Domestication and plant breeding are ongoing 10,000-year-old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.

Crop genomics: advances and applications

The completion of reference genome sequences for many important crops and the ability to perform high-throughput resequencing are providing opportunities for improving our understanding of the history of plant domestication and to accelerate crop improvement. Crop plant comparative genomics is being transformed by these data and a new generation of experimental and computational approaches. The future of crop improvement will be centred on comparisons of individual plant genomes, and some of the best opportunities may lie in using combinations of new genetic mapping strategies and evolutionary analyses to direct and optimize the discovery and use of genetic variation. Here we review such strategies and insights that are emerging.

Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach.

G. Ledyard Stebbins suggested that self-fertilization (selfing) may be an evolutionary dead end because it may result in the loss of genetic diversity and consequently preclude adaptation to changing environments. While the basic premise of selfing as a dead end is widely accepted, there have been few rigorous evaluations of the hypothesis. We examine the foundations of the dead-end hypothesis by considering theoretical advances in the study of mating-system evolution. We discuss theories predicting the irreversibility of self-fertilization and the extinction of selfing lineages through the loss of adaptive potential and genetic degradation. In the second portion of the review, focusing on the irreversibility of selfing, we summarize the contribution of phylogenetic studies of mating-system evolution to determine if evolutionary history supports this well-established hypothesis. Most studies are in accord with the hypothesis; no single study unequivocally demonstrates the transition from highly selfing to outcrossing lineages. Finally, we discuss the problems encountered when phylogenetic studies rely on reconstruction of ancestral mating systems. To avoid some of these problems, we applied likelihood ratio tests of irreversibility of mating-system evolution to several data sets and found that current data sets are probably too small for this test.

Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent

Cereal agriculture originated with the domestication of barley and early forms of wheat in the Fertile Crescent. There has long been speculation that barley was domesticated more than once. We use differences in haplotype frequency among geographic regions at multiple loci to infer at least two domestications of barley; one within the Fertile Crescent and a second 1,500–3,000 km farther east. The Fertile Crescent domestication contributed the majority of diversity in European and American cultivars, whereas the second domestication contributed most of the diversity in barley from Central Asia to the Far East.

Plant domestication, a unique opportunity to identify the genetic basis of adaptation.

Despite the fundamental role of plant domestication in human history and the critical importance of a relatively small number of crop plants to modern societies, we still know little about adaptation under domestication. Here we focus on efforts to identify the genes responsible for adaptation to domestication. We start from a historical perspective, arguing that Darwins conceptualization of domestication and unconscious selection provides valuable insight into the evolutionary history of crops and also provides a framework to evaluate modern methods used to decipher the genetic mechanisms underlying phenotypic change. We then review these methods, framing the discussion in terms of the phenotype–genotype hierarchy. Top-down approaches, such as quantitative trait locus and linkage disequilibrium mapping, start with a phenotype of interest and use genetic analysis to identify candidate genes. Bottom-up approaches, alternatively, use population genetic analyses to identify potentially adaptive genes and then rely on standard bioinformatics and reverse genetic tools to connect selected genes to a phenotype. We discuss the successes, advantages, and challenges of each, but we conclude that bottom-up approaches to understanding domestication as an adaptive process hold greater promise both for the study of adaptation and as a means to identify genes that contribute to agronomically important traits.

Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae

Single-nucleotide polymorphism was used in the construction of an expressed sequence tag map of Aegilops tauschii, the diploid source of the wheat D genome. Comparisons of the map with the rice and sorghum genome sequences revealed 50 inversions and translocations; 2, 8, and 40 were assigned respectively to the rice, sorghum, and Ae. tauschii lineages, showing greatly accelerated genome evolution in the large Triticeae genomes. The reduction of the basic chromosome number from 12 to 7 in the Triticeae has taken place by a process during which an entire chromosome is inserted by its telomeres into a break in the centromeric region of another chromosome. The original centromere–telomere polarity of the chromosome arms is maintained in the new chromosome. An intrachromosomal telomere–telomere fusion resulting in a pericentric translocation of a chromosome segment or an entire arm accompanied or preceded the chromosome insertion in some instances. Insertional dysploidy has been recorded in three grass subfamilies and appears to be the dominant mechanism of basic chromosome number reduction in grasses. A total of 64% and 66% of Ae. tauschii genes were syntenic with sorghum and rice genes, respectively. Synteny was reduced in the vicinity of the termini of modern Ae. tauschii chromosomes but not in the vicinity of the ancient termini embedded in the Ae. tauschii chromosomes, suggesting that the dependence of synteny erosion on gene location along the centromere–telomere axis either evolved recently in the Triticeae phylogenetic lineage or its evolution was recently accelerated.

Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond

Advanced resources for genome-assisted research in barley (Hordeum vulgare) including a whole-genome shotgun assembly and an integrated physical map have recently become available. These have made possible studies that aim to assess genetic diversity or to isolate single genes by whole-genome resequencing and in silico variant detection. However such an approach remains expensive given the 5 Gb size of the barley genome. Targeted sequencing of the mRNA-coding exome reduces barley genomic complexity more than 50-fold, thus dramatically reducing this heavy sequencing and analysis load. We have developed and employed an in-solution hybridization-based sequence capture platform to selectively enrich for a 61.6 megabase coding sequence target that includes predicted genes from the genome assembly of the cultivar Morex as well as publicly available full-length cDNAs and de novo assembled RNA-Seq consensus sequence contigs. The platform provides a highly specific capture with substantial and reproducible enrichment of targeted exons, both for cultivated barley and related species. We show that this exome capture platform provides a clear path towards a broader and deeper understanding of the natural variation residing in the mRNA-coding part of the barley genome and will thus constitute a valuable resource for applications such as mapping-by-sequencing and genetic diversity analyzes.

MULTILOCUS INTERACTIONS RESTRICT GENE INTROGRESSION IN INTERSPECIFIC POPULATIONS OF POLYPLOID GOSSYPIUM (COTTON)

Abstract.— Experimental advanced‐generation backcross populations contain individuals with genomic compositions similar to those resulting from interspecific hybridization in nature. By applying a detailed restriction fragment length polymorphism (RFLP) map to 3662 BC3F2 plants derived from 24 different BC1 individuals of a cross between Gossypium hirsutum and G. barbadense, large and widespread deficiencies of donor (G. barbadense) chromatin were found, and seven independent chromosomal regions were entirely absent. This skewed chromatin transmission is best accounted for by multilocus epistatic interactions affecting chromatin transmission. The observed frequencies of two‐locus genotypes were significantly different from Mendelian expectations about 26 times more often than could be explained by chance (P≤ 0.01). For identical pairs of loci, different two‐locus genotypes occurred in excess in different BC3 families, implying the existence of higher‐order interlocus interactions beyond the resolution of these data. Some G. barbadense markers occurred more frequently than expected by chance, indicating that genomic interactions do not always favor host chromatin. A preponderance of interspecific allelic interactions involved one locus each in the two different subgenomes of (allotetraploid) Gossypium, thus supporting several other lines of evidence suggesting that intersubgenomic interactions contribute to unique features that distinguish tetraploid cotton from its diploid ancestors.

Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes.

BackgroundA genome-wide assessment of nucleotide diversity in a polyploid species must minimize the inclusion of homoeologous sequences into diversity estimates and reliably allocate individual haplotypes into their respective genomes. The same requirements complicate the development and deployment of single nucleotide polymorphism (SNP) markers in polyploid species. We report here a strategy that satisfies these requirements and deploy it in the sequencing of genes in cultivated hexaploid wheat (Triticum aestivum, genomes AABBDD) and wild tetraploid wheat (Triticum turgidum ssp. dicoccoides, genomes AABB) from the putative site of wheat domestication in Turkey. Data are used to assess the distribution of diversity among and within wheat genomes and to develop a panel of SNP markers for polyploid wheat.ResultsNucleotide diversity was estimated in 2114 wheat genes and was similar between the A and B genomes and reduced in the D genome. Within a genome, diversity was diminished on some chromosomes. Low diversity was always accompanied by an excess of rare alleles. A total of 5,471 SNPs was discovered in 1791 wheat genes. Totals of 1,271, 1,218, and 2,203 SNPs were discovered in 488, 463, and 641 genes of wheat putative diploid ancestors, T. urartu, Aegilops speltoides, and Ae. tauschii, respectively. A public database containing genome-specific primers, SNPs, and other information was constructed. A total of 987 genes with nucleotide diversity estimated in one or more of the wheat genomes was placed on an Ae. tauschii genetic map, and the map was superimposed on wheat deletion-bin maps. The agreement between the maps was assessed.ConclusionsIn a young polyploid, exemplified by T. aestivum, ancestral species are the primary source of genetic diversity. Low effective recombination due to self-pollination and a genetic mechanism precluding homoeologous chromosome pairing during polyploid meiosis can lead to the loss of diversity from large chromosomal regions. The net effect of these factors in T. aestivum is large variation in diversity among genomes and chromosomes, which impacts the development of SNP markers and their practical utility. Accumulation of new mutations in older polyploid species, such as wild emmer, results in increased diversity and its more uniform distribution across the genome.