Developing maps of fitness consequences for plant genomes

Joly‐Lopez, Zoé; Flowers, Jonathan M.; Purugganan, Michael D.

doi:10.1016/j.pbi.2016.02.008

Cited by 13 publications

(12 citation statements)

References 67 publications

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“…Although a number of other methods exist to identify deleterious alleles from sequence data, GERP scores include both coding and noncoding sequence, do not require additional functional annotation, and show higher sensitivity and specificity than other related approaches [51]. While the GERP scores used here reflect conservation across relatively deep phylogenetic time, future efforts may be able to increase power by incorporating information from within-species polymorphism data [57,58] as well as other types of annotations that have been shown to contribute substantially to phenotypic variation (e.g. Wallace et al, [59] and Rodgers-Melnick et al, [50]).…”

Section: Discussionmentioning

confidence: 99%

Incomplete Dominance of Deleterious Alleles Contributes Substantially to Trait Variation and Heterosis in Maize

Yang

Mezmouk

Baumgarten

et al. 2016

Preprint

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Deleterious alleles have long been proposed to play an important role in patterning phenotypic variation and are central to commonly held ideas explaining the hybrid vigor observed in the offspring of a cross between two inbred parents. We test these ideas using evolutionary measures of sequence conservation to ask whether incorporating information about putatively deleterious alleles can inform genomic selection (GS) models and improve phenotypic prediction. We measured a number of agronomic traits in both the inbred parents and hybrids of an elite maize partial diallel population and re-sequenced the parents of the population. Inbred elite maize lines vary for more than 350,000 putatively deleterious sites, but show a lower burden of such sites than a comparable set of traditional landraces. Our modeling reveals widespread evidence for incomplete dominance at these loci, and supports theoretical models that more damaging variants are usually more recessive. We identify haplotype blocks using an identity-by-decent (IBD) analysis and perform genomic prediction analyses in which we weigh blocks on the basis of complementation for segregating putatively deleterious variants. Cross-validation results show that incorporating sequence conservation in genomic selection improves prediction accuracy for grain yield and other fitness-related traits as well as heterosis for those traits. Our results provide empirical support for an important role for incomplete dominance of deleterious alleles in explaining heterosis and demonstrate the utility of incorporating functional annotation in phenotypic prediction and plant breeding. Author summaryA key long-term goal of biology is understanding the genetic basis of phenotypic variation. Although most new mutations are likely disadvantageous, their prevalence and importance in explaining patterns of phenotypic variation is controversial and not well understood. In this study we combine whole genome-sequencing and field evaluation of a maize mapping population to investigate the contribution of deleterious mutations to phenotype. We show that a priori prediction of deleterious alleles correlates well with effect sizes for grain yield and that variants predicted to be more damaging are on average more recessive. We develop a simple model allowing for variation in the heterozygous effects of deleterious mutations and demonstrate its improved ability to predict both phenotypes and hybrid vigor. Our results help reconcile alternative explanations for hybrid vigor and highlight the use of leveraging evolutionary history to facilitate breeding for crop improvement.

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Section: Discussionmentioning

confidence: 99%

Incomplete Dominance of Deleterious Alleles Contributes Substantially to Trait Variation and Heterosis in Maize

Yang

Mezmouk

Baumgarten

et al. 2016

Preprint

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“…Germany, but its fitness was 12% of that of C24 in Norwich, UK, while both genotypes 13 showed comparable fitness in Valencia, Spain [23]. In our experiment, the Col--0 14 background generally displayed higher fitness than C24 despite temporal seasonal 15…”

Section: Cc-by-nc-ndmentioning

confidence: 48%

“…The relative fitness of the Col--0 and C24 backgrounds were reported to change markedly 11 across geographical sites [23]. The Col--0 genotype produced 50% more siliques in Halle, 12…”

Section: Cc-by-nc-ndmentioning

confidence: 99%

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Temporal fitness fluctuations in experimentalArabidopsis thalianapopulations

Hu¹,

Meaux

2017

Preprint

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Understanding the genetics of lifetime fitness is crucial to understand a species’ ecological preferences and ultimately predict its ability to cope with novel environmental conditions. Yet, there is a dearth of information regarding the impact of the ecological variance experienced by natural populations on expressed phenotypic and fitness differences. Here, we follow the natural dynamics of experimental A. thaliana populations over 5 successive plantings whose timing was determined by the natural progression of the plant’s life cycle and disentangle the environmental and genetic factors that drive plant ecological performance at a given locality. We show that, at the intermediate latitude where the experiment was conducted, a given genotype can experience different life cycles across successive seasons. Lifetime fitness across these seasons varied strongly, with a fall planting yielding 36-fold higher fitness compared to a spring planting. In addition, the actual life-stage at which plant overwinter oscillated across years, depending on the timing of the end of the summer season. We observed a rare but severe fitness differential after inadequate early flowering in one of the five planting. Substrate variation played a comparatively minor role, but also contributed to modulate the magnitude of fitness differentials between genotypes. Finally, reciprocal introgressions on chromosome 4 demonstrated that the fitness effect of a specific chromosomal region is strongly contingent on micro-geographic and seasonal fluctuations. Our study contributes to emphasize the extent to which the fitness impact of phenotypic traits and the genes that encode them in the genome can fluctuate. Experiments aiming at dissecting the molecular basis of local adaptation must apprehend the complexity introduced by temporal fluctuations because they massively affect the expression of phenotype and fitness differences.

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“…Annotating how functions encoded in the genome impact ecological performance and fitness seems within reach [45]. Our findings, however, have important bearings on the challenges we are facing for plant (or animal) species that can shift their temporal niches across generations.…”

Section: Resultsmentioning

confidence: 99%

Temporal fitness fluctuations in experimental Arabidopsis thaliana populations

Meaux

2017

PLoS ONE

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Understanding the genetics of lifetime fitness is crucial to understand a species’ ecological preferences and ultimately predict its ability to cope with novel environmental conditions. Yet, there is a dearth of information regarding the impact of the ecological variance experienced by natural populations on expressed phenotypic and fitness differences. Here, we follow the natural dynamics of experimental A. thaliana populations over 5 successive plantings whose timing was determined by the natural progression of the plant’s life cycle and disentangle the environmental and genetic factors that drive plant ecological performance at a given locality. We show that, at the temperate latitude where the experiment was conducted, a given genotype can experience winter-, spring- or summer-annual life cycles across successive seasons. Lifetime fitness across these seasons varied strongly, with a fall planting yielding 36-fold higher fitness compared to a spring planting. In addition, the actual life-stage at which plant overwinter oscillated across years, depending on the timing of the end of the summer season. We observed a rare but severe fitness differential coinciding with inadequate early flowering in one of the five planting. Substrate variation played a comparatively minor role, but also contributed to modulate the magnitude of fitness differentials between genotypes. Finally, reciprocal introgressions on chromosome 4 demonstrated that the fitness effect of a specific chromosomal region is strongly contingent on micro-geographic and seasonal fluctuations. Our study contributes to emphasize the extent to which the fitness impact of phenotypic traits and the genes that encode them in the genome can fluctuate. Experiments aiming at dissecting the molecular basis of local adaptation must apprehend the complexity introduced by temporal fluctuations because they massively affect the expression of phenotype and fitness differences.

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Developing maps of fitness consequences for plant genomes

Cited by 13 publications

References 67 publications

Incomplete Dominance of Deleterious Alleles Contributes Substantially to Trait Variation and Heterosis in Maize

Incomplete Dominance of Deleterious Alleles Contributes Substantially to Trait Variation and Heterosis in Maize

Temporal fitness fluctuations in experimentalArabidopsis thalianapopulations

Temporal fitness fluctuations in experimental Arabidopsis thaliana populations

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