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      Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize

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          Abstract

          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 summary

          A 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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          Most cited references41

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          Introduction to Quantitative Genetics

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            The genetics of inbreeding depression.

            Inbreeding depression - the reduced survival and fertility of offspring of related individuals - occurs in wild animal and plant populations as well as in humans, indicating that genetic variation in fitness traits exists in natural populations. Inbreeding depression is important in the evolution of outcrossing mating systems and, because intercrossing inbred strains improves yield (heterosis), which is important in crop breeding, the genetic basis of these effects has been debated since the early twentieth century. Classical genetic studies and modern molecular evolutionary approaches now suggest that inbreeding depression and heterosis are predominantly caused by the presence of recessive deleterious mutations in populations.
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              New mini- zincin structures provide a minimal scaffold for members of this metallopeptidase superfamily

              Background The Acel_2062 protein from Acidothermus cellulolyticus is a protein of unknown function. Initial sequence analysis predicted that it was a metallopeptidase from the presence of a motif conserved amongst the Asp-zincins, which are peptidases that contain a single, catalytic zinc ion ligated by the histidines and aspartic acid within the motif (HEXXHXXGXXD). The Acel_2062 protein was chosen by the Joint Center for Structural Genomics for crystal structure determination to explore novel protein sequence space and structure-based function annotation. Results The crystal structure confirmed that the Acel_2062 protein consisted of a single, zincin-like metallopeptidase-like domain. The Met-turn, a structural feature thought to be important for a Met-zincin because it stabilizes the active site, is absent, and its stabilizing role may have been conferred to the C-terminal Tyr113. In our crystallographic model there are two molecules in the asymmetric unit and from size-exclusion chromatography, the protein dimerizes in solution. A water molecule is present in the putative zinc-binding site in one monomer, which is replaced by one of two observed conformations of His95 in the other. Conclusions The Acel_2062 protein is structurally related to the zincins. It contains the minimum structural features of a member of this protein superfamily, and can be described as a “mini- zincin”. There is a striking parallel with the structure of a mini-Glu-zincin, which represents the minimum structure of a Glu-zincin (a metallopeptidase in which the third zinc ligand is a glutamic acid). Rather than being an ancestral state, phylogenetic analysis suggests that the mini-zincins are derived from larger proteins.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: Resources
                Role: ResourcesRole: Writing – review & editing
                Role: Data curationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                September 2017
                27 September 2017
                : 13
                : 9
                : e1007019
                Affiliations
                [1 ] Department of Plant Sciences, University of California, Davis, Davis, California, United States of America
                [2 ] DuPont Pioneer, Johnston, Iowa, United States of America
                [3 ] School of Integrative Plant Sciences, Section of Plant Breeding and Genetics, Cornell University, Ithaca, New York, United States of America
                [4 ] Institute for Genomic Diversity, Ithaca, New York, United States of America
                [5 ] US Department of Agriculture–Agricultural Research Service, Ithaca, New York, United States of America
                [6 ] US Department of Agriculture, Agricultural Research Service, Columbia, Missouri, United States of America
                [7 ] Division of Plant Sciences, University of Missouri, Columbia, Missouri, United States of America
                [8 ] Department of Crop Sciences and the Illinois Plant Breeding Center, University of Illinois at Urbana-Champaign, Urbana, Illinois, United States of America
                [9 ] Center for Population Biology and Genome Center, University of California, Davis, California, United States of America
                University of Rochester, UNITED STATES
                Author notes

                I have read the journal’s policy and the authors of this manuscript have the following competing interests: Rita Mumm received research funding from Kellogg Company to support field work, equipment, and travel. She is a paid consultant for Mars Inc. and serves on the leadership team of the African Orphan Crop Consortium which is funded in part by Mars Inc. Jeffrey Ross-Ibarra received research funding from DuPont Pioneer and Mars Inc. Sofiane Mezmouk is a current employee of KWS. Andy Baumgarten is a current employee of DuPont Pioneer. All authors declare no additional competing interests, and none of the funders played any role in the study design; collection, analysis, and interpretation of data; writing of the paper; and/or decision to submit for publication.

                [¤a]

                Current address: Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America

                [¤b]

                Current address: KWS SAAT SE, Einbeck, Germany

                Author information
                http://orcid.org/0000-0002-0999-3518
                http://orcid.org/0000-0001-5766-2732
                http://orcid.org/0000-0002-3100-371X
                http://orcid.org/0000-0001-9339-2290
                Article
                PGENETICS-D-16-02825
                10.1371/journal.pgen.1007019
                5633198
                28953891
                e2b55a91-8720-4ebd-8f9a-ad29cfb3c74c
                © 2017 Yang et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 22 December 2016
                : 13 September 2017
                Page count
                Figures: 3, Tables: 0, Pages: 21
                Funding
                Financial support for this work came from NSF (grants IOS-0820619 and IOS-1238014), USDA (grant 2009-65300-05668 and Hatch projects CA-D-PLS-2066-H and ILLU-802-354), DuPont Pioneer, Kellogg Company, and Mars Incorporated. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Genetics
                Genetic Loci
                Alleles
                Biology and Life Sciences
                Genetics
                Heredity
                Heterosis
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Maize
                Research and Analysis Methods
                Model Organisms
                Maize
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Maize
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
                Maize
                Biology and Life Sciences
                Genetics
                Genomics
                Plant Genomics
                Biology and Life Sciences
                Biotechnology
                Plant Biotechnology
                Plant Genomics
                Biology and Life Sciences
                Plant Science
                Plant Biotechnology
                Plant Genomics
                Biology and Life Sciences
                Genetics
                Plant Genetics
                Plant Genomics
                Biology and Life Sciences
                Plant Science
                Plant Genetics
                Plant Genomics
                Biology and Life Sciences
                Genetics
                Phenotypes
                Biology and Life Sciences
                Genetics
                Heredity
                Inbreeding
                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Forecasting
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Statistical Methods
                Forecasting
                Biology and Life Sciences
                Genetics
                Molecular Genetics
                Biology and Life Sciences
                Molecular Biology
                Molecular Genetics
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-10-09
                Sequencing data have been deposited in NCBI SRA (SRP103329) database, and code for all analyses are available in the public GitHub repository ( https://github.com/yangjl/GERP-diallel).

                Genetics
                Genetics

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