Patterns of Molecular Evolution Associated With Two Selective Sweeps in the <i>Tb1</i>–<i>Dwarf8</i> Region in Maize

Camus-Kulandaivelu, Létizia; Chevin, Luis‐Miguel; Tollon-Cordet, Christine; Charcosset, Alain; Manicacci, Doménica; Tenaillon, Maud I.

doi:10.1534/genetics.108.088849

Cited by 33 publications

(21 citation statements)

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“…Finally, note that the KZ and Q1KZ models show many more cases of no convergence than other mixed models. The mixed model had been extensively used for the highly structured phenotype of flowering date GonzalezMartinez et al, 2007;Zhao et al, 2007;Camus-Kulandaivelu et al, 2008). Our study confirms its efficiency in excluding false positives for kernel quality traits, and we consider that both population structure and individual kinship should be included in association studies of all phenotypic traits with candidate genes.…”

Section: Association Geneticssupporting

confidence: 78%

Epistatic Interactions betweenOpaque2Transcriptional Activator and Its Target GeneCyPPDK1Control Kernel Trait Variation in Maize

Manicacci¹,

Camus-Kulandaivelu²,

Fourmann³

et al. 2009

Plant Physiology

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Association genetics is a powerful method to track gene polymorphisms responsible for phenotypic variation, since it takes advantage of existing collections and historical recombination to study the correlation between large genetic diversity and phenotypic variation. We used a collection of 375 maize (Zea mays ssp. mays) inbred lines representative of tropical, American, and European diversity, previously characterized for genome-wide neutral markers and population structure, to investigate the roles of two functionally related candidate genes, Opaque2 and CyPPDK1, on kernel quality traits. Opaque2 encodes a basic leucine zipper transcriptional activator specifically expressed during endosperm development that controls the transcription of many target genes, including CyPPDK1, which encodes a cytosolic pyruvate orthophosphate dikinase. Using statistical models that correct for population structure and individual kinship, Opaque2 polymorphism was found to be strongly associated with variation of the essential amino acid lysine. This effect could be due to the direct role of Opaque2 on either zein transcription, zeins being major storage proteins devoid of lysine, or lysine degradation through the activation of lysine ketoglutarate reductase. Moreover, we found that a polymorphism in the Opaque2 coding sequence and several polymorphisms in the CyPPDK1 promoter nonadditively interact to modify both lysine content and the protein-versus-starch balance, thus revealing the role in quantitative variation in plants of epistatic interactions between a transcriptional activator and one of its target genes.

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Section: Association Geneticssupporting

confidence: 78%

Epistatic Interactions betweenOpaque2Transcriptional Activator and Its Target GeneCyPPDK1Control Kernel Trait Variation in Maize

Manicacci¹,

Camus-Kulandaivelu²,

Fourmann³

et al. 2009

Plant Physiology

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“…Perhaps more readily, the search for interfering selective sweeps could be helpful in specific studies focusing on smaller candidate regions, in which several putative targets of selection have already been identified. In such cases, the analysis of the polymorphism pattern could provide information not only about the presence of selection, but also about the synchronicity of selective sweeps or the origin (migration vs. mutation) of beneficial alleles This could yield valuable insights into the adaptive history of a species (Camus-Kulandaivelu et al 2008).…”

Section: Discussionmentioning

confidence: 99%

“…The first one concerns two genes involved in sex-ratio distortion in Drosophila simulans (Derome et al 2008). The second one deals with the domestication gene Tb1 and the early-flowering gene dwarf8 in maize (Camus-Kulandaivelu et al 2008). These two studies at least suggest that successful selective sweeps at two tightly linked loci can occur in natural populations.…”

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confidence: 99%

Hitchhiking Both Ways: Effect of Two Interfering Selective Sweeps on Linked Neutral Variation

Chevin

Billiard

2008

Genetics

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The neutral polymorphism pattern in the vicinity of a selective sweep can be altered by both stochastic and deterministic factors. Here, we focus on the impact of another selective sweep in the region of influence of a first one. We study the signature left on neutral polymorphism by positive selection at two closely linked loci, when both beneficial mutations reach fixation. We show that, depending on the timing of selective sweeps and on their selection coefficients, the two hitchhiking effects can interfere with each other, leading to less reduction in heterozygosity than a single selective sweep of the same magnitude and more importantly to an excess of intermediate-frequency variants relative to neutrality under some parameter values. This pattern can be sustained and potentially alter the detection of positive selection, including by provoking spurious detection of balancing selection. In situations where positive selection is suspected a priori at several closely linked loci, the polymorphism pattern in the region may also be informative about their selective histories.T HE search for molecular signatures of positive selection has been a matter of intense research and applications in the recent years, motivated by the hope to better understand the genetic bases of adaptation and the recent history of populations (Bamshad and Wooding 2003;Nielsen et al. 2007). The footprints of positive selection on neutral polymorphism are the consequence of the hitchhiking effect (Maynard Smith and Haigh 1974), and current methods to detect them encompass two main approaches. The first one is genome scans of neutral variation and is a top-down process. It consists of gathering polymorphism data widely distributed throughout the genome and summarizing them with a particular measure, be it the nucleotide diversity, the frequency spectrum of mutations (Nielsen et al. 2005), or the length and frequency of haplotypes [for ongoing selective sweeps (Sabeti et al. 2002; Voight et al. 2006)]. The loci exhibiting extreme values in the distribution of the measure are then considered as putative targets of positive selection (but see Teshima et al. 2006 for caveats of this method). The second approach, the candidate-gene approach, is a bottom-up process in which one wishes to test some evolutionary scenarios, for instance, for a gene (or QTL) of known function (see, for instance, Edelist et al. 2006). It consists of analyzing neutral polymorphism at a finer scale (of the order of the megabase or lower), to test if positive selection occurred, and to infer some parameters of the selective sweep such as the target and strength of selection. This fine-scale analysis can also be carried out in regions identified after a genome scan (a good example of this kind is Pool et al. 2006; for a more comprehensive review see . Here, we focus on this finer-scale analysis of polymorphism.The most popular method for the fine-scale analysis of selective sweeps uses the information at several markers distributed in the small region of interes...

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“…Although there is some evidence for multiple functional elements in tb1, the major element is 60 kb upstream of the gene (41). There is also evidence for a second, distant interfering sweep at this locus (42). The timing and sequence of such character selection by early farmers is now being revealed by the fusion of molecular biology and archaeological research.…”

Section: What Were the Steps Of Domestication Like?mentioning

confidence: 99%

Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10

Tian

Stevens

Buckler

2009

Proc. Natl. Acad. Sci. U.S.A.

134

121

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Maize domestication is one of the greatest feats of artificial selection and evolution, wherein a weedy plant in Central Mexico was converted through human-mediated selection into the most productive crop in the world. In fact, the changes were so astounding that it took much of the last century to identify modern maize's true ancestor. Through modern genetic studies, the molecular basis of this evolution is being unraveled. Maize's new morphology and adaptation to diverse environments required selection at thousands of loci, and we are beginning to understand the magnitude and rates of these genetic changes. Most of the known major genes have experienced strong selection, but only small regions surrounding the selected genes exhibit substantially reduced genetic diversity. Here, we report the discovery of a large region on chromosome 10 involved in adaptation or domestication that has been the target of strong selection during maize domestication. Unlike previously described regions in the maize genome, 1.1 Mb and >15 genes lost genetic diversity during selection at this region. Finally, the prospects of a detailed understanding of maize evolution are discussed with consideration of both top-down and bottom-up approaches.Although man does not cause variability and cannot even prevent it, he can select, preserve, and accumulate the variations given to him by the hand of nature almost in any way that he chooses; and thus he can certainly produce a great result.Charles Darwin (1) W ith its meager ear containing only 2 entwined rows of well-armored kernels, teosinte grows on Mexican hillsides. This grass might easily have been overlooked were it not for its abundant variation, a gift not lost on early agriculturists. Within the last 10,000 years, early Native Americans were able to transform teosinte into a plant whose ears would feed the world. It was a transformation so striking and so complex that some researchers did not believe it was possible, leading to years of competing theories and intense debate. But as Darwin himself recognized, when the desires of humans meet the diversity of nature the result can indeed be astounding.The molecular revolution of the last 2 decades has provided compelling evidence that teosinte is the progenitor of modern maize. Here, we discuss the rich genetic diversity at the source of this morphological conversion and examine how human selection has impacted this diversity. One key question concerning maize domestication remains to be resolved: was maize domestication the result of selection on a small number of loci with large effects, a large number of loci with small effects, or both? Recent genetic evidence has provided clues about the relative contributions of large-effect and small-effect loci. We discuss how future studies will help unravel the mysteries surrounding maize domestication and how this information is key to future improvements of maize.

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Patterns of Molecular Evolution Associated With Two Selective Sweeps in the Tb1–Dwarf8 Region in Maize

Cited by 33 publications

References 84 publications

Epistatic Interactions betweenOpaque2Transcriptional Activator and Its Target GeneCyPPDK1Control Kernel Trait Variation in Maize

Epistatic Interactions betweenOpaque2Transcriptional Activator and Its Target GeneCyPPDK1Control Kernel Trait Variation in Maize

Hitchhiking Both Ways: Effect of Two Interfering Selective Sweeps on Linked Neutral Variation

Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10

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