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A Bountiful Harvest: Genomic Insights into Crop Domestication Phenotypes
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Human selection during crop domestication has resulted in remarkable transformations of plant phenotypes, providing a window into the genetic basis of morphological evolution. Recent progress in our understanding of the genetic architecture of novel plant traits has emerged from combining advanced molecular technologies with improved experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies reveal a diversity of underlying causative mutations affecting phenotypes important in plant domestication and crop improvement, including coding sequence substitutions, presence/absence and copy number variation, transposon activation leading to novel gene structures and expression patterns, diversification following gene duplication, and polyploidy leading to altered combinatorial capabilities. The genomic regions unknowingly targeted by human selection include both structural and regulatory genes, often with results that propagate through the transcriptome as well as to other levels in the biosynthetic and morphogenetic networks. Expected final online publication date for the Annual Review of Plant Biology Volume 64 is April 29, 2013. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
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Polyploidy is a prominent mechanism of plant speciation and adaptation, yet the mechanistic understandings of duplicated gene regulation remain elusive. Chromatin structure dynamics are suggested to govern gene regulatory control. Here we characterized genome-wide nucleosome organization and chromatin accessibility in allotetraploid cotton, Gossypium hirsutum (AADD, 2n=4X=52), relative to its two diploid parents (AA or DD genome) and their synthetic diploid hybrid (AD), using DNS-seq. The larger A-genome exhibited wider average nucleosome spacing in diploids, and this inter-genomic difference diminished in the allopolyploid but not hybrid. Allopolyploidization also exhibited increased accessibility at promoters genome-wide and synchronized cis-regulatory motifs between subgenomes. A prominent cis-acting control was inferred for chromatin dynamics and demonstrated by transposable element removal from promoters. Linking accessibility to gene expression patterns, we found distinct regulatory effects for hybridization and later allopolyploid stages, including nuanced establishment of homoeolog expression bias and expression level dominance. Histone gene expression and nucleosome organization are coordinated through chromatin accessibility. Our study demonstrates the capability to track high resolution chromatin structure dynamics and reveals their role in the evolution of cis-regulatory landscapes and duplicate gene expression in polyploids, illuminating regulatory ties to subgenomic asymmetry and dominance.
As sessile organisms, plants must respond constantly to ever-changing environments to complete their life cycle; this includes the transition from vegetative growth to reproductive development. This process is mediated by photoperiodic response to sensing the length of night or day through circadian regulation of light-signaling molecules, such as phytochromes, to measure the length of night to initiate flowering. Flowering time is the most important trait to optimize crop performance in adaptive regions. In this review, we focus on interplays between circadian and light signaling pathways that allow plants to optimize timing for flowering and seed production in Arabidopsis, rice, soybean, and cotton. Many crops are polyploids and domesticated under natural selection and breeding. In response to adaptation and polyploidization, circadian and flowering pathway genes are epigenetically reprogrammed. Understanding the genetic and epigenetic bases for photoperiodic flowering will help improve crop yield and resilience in response to climate change.
Flowering time and growth period are key agronomic traits which directly affect soybean ( Glycine max (L.) Merr.) adaptation to diverse latitudes and farming systems. The FLOWERING LOCUS T (FT) homologs GmFT2a and GmFT5a integrate multiple flowering regulation pathways and significantly advance flowering and maturity in soybean. Pinpointing the genes responsible for regulating GmFT2a and GmFT5a will improve our understanding of the molecular mechanisms governing growth period in soybean. In this study, we identified the Nuclear Factor Y‐C (NFY‐C) protein GmNF‐YC4 as a novel flowering suppressor in soybean under long‐day (LD) conditions. GmNF‐YC4 delays flowering and maturation by directly repressing the expression of GmFT2a and GmFT5a . In addition, we found that a strong selective sweep event occurred in the chromosomal region harboring the GmN F‐YC4 gene during soybean domestication. The GmNF‐YC4 Hap3 allele was mainly found in wild soybean ( Glycine soja Siebold & Zucc.) and has been eliminated from G. max landraces and improved cultivars, which predominantly contain the GmNF‐YC4 Hap1 allele. Furthermore, the Gmnf‐yc4 mutants displayed notably accelerated flowering and maturation under LD conditions. These alleles may prove to be valuable genetic resources for enhancing soybean adaptability to higher latitudes.
The origin and functionality of long noncoding RNA (lncRNA) remain poorly understood. Here, we show that multiple quantitative trait loci modulating distinct domestication traits in soybeans are pleiotropic effects of a locus composed of two tandem lncRNA genes. These lncRNA genes, each containing two inverted repeats, originating from coding sequences of the MYB genes, function in wild soybeans by generating clusters of small RNA (sRNA) species that inhibit the expression of their MYB gene relatives through post-transcriptional regulation. By contrast, the expression of lncRNA genes in cultivated soybeans is severely repressed, and, consequently, the corresponding MYB genes are highly expressed, shaping multiple distinct domestication traits as well as leafhopper resistance. The inverted repeats were formed before the divergence of the Glycine genus from the Phaseolus–Vigna lineage and exhibit strong structure–function constraints. This study exemplifies a type of target for selection during plant domestication and identifies mechanisms of lncRNA formation and action.
Modern agricultural operations employ crop improvement methods that have paradoxically diminished the genetic diversity of crop plants. Traditional crop development processes aimed at managing biotic and abiotic stresses often employ common genes, alleles, or parent lines, rendering them more susceptible to rapid failure. Contrarily, landraces of customary agricultural plants have consistently demonstrated resilience against unfavourable climatic conditions despite being limited to marginal areas. These landraces possess a substantial genetic potential that can be harnessed in pre-breeding or other plant breeding activities. Efforts are ongoing to preserve this genetic potential through on-farm, in-situ, or ex-situ conservation. Gene introgression into new varieties from landraces has shown promise. This is achieved through genomic selection based on the phenotypic and/or genotypic screening of desired traits. Modern molecular plant breeding tools such as QTL mapping and marker-assisted selection, alongside biotechnological tools for gene pyramiding, can be employed to prepare parental lines for crosses or to directly introduce them into a desired cultivar. Mutation breeding, an emerging tool in plant breeding, has shown considerable promise. It is now used with high throughput screening and/or genomic selection to identify beneficial heritable changes at the genome level with precision and speed. Given that rural landraces are reservoirs of extensive genetic variability, tools like mutation breeding can facilitate more significant deviations among the parentage of newly developed crops. Genetic homogeneity among crops poses an inherent risk when exposed to pertinent biotic or abiotic factors, potentially leading to total crop failure. Thus, the ultimate aim of new-age plant breeding programs is strategically exploiting and utilizing landraces. This is achieved by extending plant breeding activities, and leveraging new generation technology to expedite the process with greater precision, thereby enhancing the development of rural landraces through mutation breeding.
Asian rice, Oryza sativa is a cultivated, inbreeding species that feeds over half of the world's population. Understanding the genetic basis of diverse physiological, developmental, and morphological traits provides the basis for improving yield, quality and sustainability of rice. Here we show the results of a genome-wide association study based on genotyping 44,100 SNP variants across 413 diverse accessions of O. sativa collected from 82 countries that were systematically phenotyped for 34 traits. Using cross-population-based mapping strategies, we identified dozens of common variants influencing numerous complex traits. Significant heterogeneity was observed in the genetic architecture associated with subpopulation structure and response to environment. This work establishes an open-source translational research platform for genome-wide association studies in rice that directly links molecular variation in genes and metabolic pathways with the germplasm resources needed to accelerate varietal development and crop improvement.
Darwin studied domesticated plants and animals to try to understand the causes of variability. He observed that variation is greatest in the part of the plant most used by humans, but explanations of the causes of this variation had to await the discovery of Mendelian genetics and subsequent advances in the understanding of the structure and mode of action of genes, from the one gene, one enzyme hypothesis to the role of transcriptional regulators. Darwin credited his studies on domesticated plants and animals with demonstrating to him the power of selection. He recognized two forms of human-mediated selection, methodical and unconscious, in addition to natural selection. Selection leaves a signature in the form of reduced diversity in genes that have been the targets of selection and in 'hitch-hiking' genomic regions linked to the target genes. These so-called selective sweeps may serve now to identify genes targeted by selection in early stages of domestication and thus provide a possible guide to crop improvement in future. (C) 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 203-212.
The domestication of all major crop plants occurred during a brief period in human history about 10,000 years ago. During this time, ancient agriculturalists selected seed of preferred forms and culled out seed of undesirable types to produce each subsequent generation. Consequently, favoured alleles at genes controlling traits of interest increased in frequency, ultimately reaching fixation. When selection is strong, domestication has the potential to drastically reduce genetic diversity in a crop. To understand the impact of selection during maize domestication, we examined nucleotide polymorphism in teosinte branched1, a gene involved in maize evolution. Here we show that the effects of selection were limited to the gene's regulatory region and cannot be detected in the protein-coding region. Although selection was apparently strong, high rates of recombination and a prolonged domestication period probably limited its effects. Our results help to explain why maize is such a variable crop. They also suggest that maize domestication required hundreds of years, and confirm previous evidence that maize was domesticated from Balsas teosinte of southwestern Mexico.
Plant genomes vary in size and complexity, fueled in part by processes of whole-genome duplication (WGD; polyploidy) and subsequent genome evolution. Despite repeated episodes of WGD throughout the evolutionary history of angiosperms in particular, the genomes are not uniformly large, and even plants with very small genomes carry the signatures of ancient duplication events. The processes governing the evolution of plant genomes following these ancient events are largely unknown. Here, we consider mechanisms of diploidization, evidence of genome reorganization in recently formed polyploid species, and macroevolutionary patterns of WGD in plant genomes and propose that the ongoing genomic changes observed in recent polyploids may illustrate the diploidization processes that result in ancient signatures of WGD over geological timescales.
Advances in next generation technologies have driven the costs of DNA sequencing down to the point that genotyping-by-sequencing (GBS) is now feasible for high diversity, large genome species. Here, we report a procedure for constructing GBS libraries based on reducing ...
... In Plant Speciation , Grant (1981) devoted five chapters (15% of the total text) to polyploidy, reflecting the importance of the topic both to the author and to plant biologists. We update Grant's (1981) coverage by highlighting some ...
... [Because an autopolyploid may arise via crossing between genetically different individuals (179, 195), the concept of hybridization may extend to autopolyploids as well (17, 72), and we therefore include autopolyploidy in this review.] Thus, an autotetraploid will contain four ...