Publications by authors named "Zoë Migicovsky"

28 Publications

  • Page 1 of 1

Apple Ripening Is Controlled by a NAC Transcription Factor.

Front Genet 2021 22;12:671300. Epub 2021 Jun 22.

Department of Plant, Food and Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada.

Softening is a hallmark of ripening in fleshy fruits, and has both desirable and undesirable implications for texture and postharvest stability. Accordingly, the timing and extent of pre-harvest ripening and associated textural changes following harvest are key targets for improving fruit quality through breeding. Previously, we identified a large effect locus associated with harvest date and firmness in apple () using genome-wide association studies (GWAS). Here, we present additional evidence that polymorphisms in or around a transcription factor gene, , may cause variation in these traits. First, we confirmed our previous findings with new phenotype and genotype data from ∼800 apple accessions. In this population, we compared a genetic marker within to markers targeting three other firmness-related genes currently used by breeders (, , and ), and found that the marker was the strongest predictor of both firmness at harvest and firmness after 3 months of cold storage. By sequencing across 18 accessions, we revealed two predominant haplotypes containing the single nucleotide polymorphism (SNP) previously identified using GWAS, as well as dozens of additional SNPs and indels in both the coding and promoter sequences. encodes a protein that is orthogolous to the NON-RIPENING (NOR) transcription factor, a regulator of ripening in tomato (). We introduced both transgene haplotypes into the tomato mutant and showed that both haplotypes complement the ripening deficiency. Taken together, these results indicate that polymorphisms in may underlie substantial variation in apple firmness through modulation of a conserved ripening program.
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http://dx.doi.org/10.3389/fgene.2021.671300DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8258254PMC
June 2021

Genome-Wide Association Study Reveals Genomic Region Associated with Mite-Recruitment Phenotypes in the Domesticated Grapevine ().

Genes (Basel) 2021 Jun 30;12(7). Epub 2021 Jun 30.

Department of Plant Biology, Program in Ecology, Evolution, and Behavior, Michigan State University, East Lansing, MI 48824, USA.

Indirect defenses are plant phenotypes that reduce damage by attracting natural enemies of plant pests and pathogens to leaves. Despite their economic and ecological importance, few studies have investigated the genetic underpinnings of indirect defense phenotypes. Here, we present a genome-wide association study of five phenotypes previously determined to increase populations of beneficial (fungivorous and predacious) mites on grape leaves (genus ): leaf bristles, leaf hairs, and the size, density, and depth of leaf domatia. Using a common garden genetic panel of 399 cultivars, we tested for genetic associations of these phenotypes using previously obtained genotyping data from the Vitis9kSNP array. We found one single nucleotide polymorphism (SNP) significantly associated with domatia density. This SNP (Chr5:1160194) is near two genes of interest: (VIT_205s0077g01440), involved in downy mildew resistance, and (VIT_205s0077g01450), involved in leaf shape development. Our findings are among the first to examine the genomic regions associated with ecologically important plant traits that facilitate interactions with beneficial mites, and suggest promising candidate genes for breeding and genetic editing to increase naturally occurring predator-based defenses in grapevines.
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http://dx.doi.org/10.3390/genes12071013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8307218PMC
June 2021

Grapevine rootstocks affect growth-related scion phenotypes.

Plant Direct 2021 May 27;5(5):e00324. Epub 2021 May 27.

Department of Horticulture Michigan State University East Lansing MI USA.

Grape growers use rootstocks to provide protection against pests and pathogens and to modulate viticulture performance such as shoot growth. Our study examined two grapevine scion varieties ('Chardonnay' and 'Cabernet Sauvignon') grafted to 15 different rootstocks and determined the effect of rootstocks on eight traits important to viticulture. We assessed the vines across five years and identified both year and variety as contributing strongly to trait variation. The effect of rootstock was relatively consistent across years and varieties, explaining between 8.99% and 9.78% of the variation in growth-related traits including yield, pruning weight, berry weight and Ravaz index (yield to pruning weight ratio). Increases in yield due to rootstock were generally the result of increases in berry weight, likely due to increased water uptake by vines grafted to a particular rootstock. We demonstrated a greater than 50% increase in yield, pruning weight, or Ravaz index by choosing the optimal rootstock, indicating that rootstock choice is crucial for grape growers looking to improve vine performance.
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http://dx.doi.org/10.1002/pld3.324DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8156960PMC
May 2021

Vein-to-blade ratio is an allometric indicator of leaf size and plasticity.

Am J Bot 2021 04;108(4):571-579

U.S. Department of Agriculture, Agriculture Research Service, Grape Genetics Research Unit, Geneva, NY, 14456, USA.

Premise: As a leaf expands, its shape dynamically changes. Previously, we documented an allometric relationship between vein and blade area in grapevine leaves. Larger leaves have a smaller ratio of primary and secondary vein area relative to blade area compared to smaller leaves. We sought to use allometry as an indicator of leaf size and plasticity.

Methods: We measured the ratio of vein-to-blade area from the same 208 vines across four growing seasons (2013, 2015, 2016, and 2017). Matching leaves by vine and node, we analyzed the correlation between the size and shape of grapevine leaves as repeated measures with climate variables across years.

Results: The proportion of leaf area occupied by vein and blade exponentially decreased and increased, respectively, during leaf expansion making their ratio a stronger indicator of leaf size than area itself. Total precipitation and leaf wetness hours of the previous year but not the current showed strong negative correlations with vein-to-blade ratio, whereas maximum air temperature from the previous year was positively correlated.

Conclusions: Our results demonstrate that vein-to-blade ratio is a strong allometric indicator of leaf size and plasticity in grapevines measured across years. Grapevine leaf primordia are initiated in buds the year before they emerge, and we found that total precipitation and maximum air temperature of the previous growing season exerted the largest statistically significant effects on leaf morphology. Vein-to-blade ratio is a promising allometric indicator of relationships between leaf morphology and climate, the robustness of which should be explored further.
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http://dx.doi.org/10.1002/ajb2.1639DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8252563PMC
April 2021

Genomic consequences of apple improvement.

Hortic Res 2021 Jan 1;8(1). Epub 2021 Jan 1.

Department of Plant, Food, and Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada.

The apple (Malus domestica) is one of the world's most commercially important perennial crops and its improvement has been the focus of human effort for thousands of years. Here, we genetically characterise over 1000 apple accessions from the United States Department of Agriculture (USDA) germplasm collection using over 30,000 single-nucleotide polymorphisms (SNPs). We confirm the close genetic relationship between modern apple cultivars and their primary progenitor species, Malus sieversii from Central Asia, and find that cider apples derive more of their ancestry from the European crabapple, Malus sylvestris, than do dessert apples. We determine that most of the USDA collection is a large complex pedigree: over half of the collection is interconnected by a series of first-degree relationships. In addition, 15% of the accessions have a first-degree relationship with one of the top 8 cultivars produced in the USA. With the exception of 'Honeycrisp', the top 8 cultivars are interconnected to each other via pedigree relationships. The cultivars 'Golden Delicious' and 'Red Delicious' were found to have over 60 first-degree relatives, consistent with their repeated use by apple breeders. We detected a signature of intense selection for red skin and provide evidence that breeders also selected for increased firmness. Our results suggest that Americans are eating apples largely from a single family tree and that the apple's future improvement will benefit from increased exploitation of its tremendous natural genetic diversity.
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http://dx.doi.org/10.1038/s41438-020-00441-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7775473PMC
January 2021

Composite modeling of leaf shape along shoots discriminates species better than individual leaves.

Appl Plant Sci 2020 Dec 3;8(12):e11404. Epub 2020 Dec 3.

Department of Horticulture Michigan State University East Lansing Michigan 48824 USA.

Premise: Leaf morphology is dynamic, continuously deforming during leaf expansion and among leaves within a shoot. Here, we measured the leaf morphology of more than 200 grapevines ( spp.) over four years and modeled changes in leaf shape along the shoot to determine whether a composite leaf shape comprising all the leaves from a single shoot can better capture the variation and predict species identity compared with individual leaves.

Methods: Using homologous universal landmarks found in grapevine leaves, we modeled various morphological features as polynomial functions of leaf nodes. The resulting functions were used to reconstruct modeled leaf shapes across the shoots, generating composite leaves that comprehensively capture the spectrum of leaf morphologies present.

Results: We found that composite leaves are better predictors of species identity than individual leaves from the same plant. We were able to use composite leaves to predict the species identity of previously unassigned grapevines, which were verified with genotyping.

Discussion: Observations of individual leaf shape fail to capture the true diversity between species. Composite leaf shape-an assemblage of modeled leaf snapshots across the shoot-is a better representation of the dynamic and essential shapes of leaves, in addition to serving as a better predictor of species identity than individual leaves.
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http://dx.doi.org/10.1002/aps3.11404DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7742203PMC
December 2020

Saltmarsh rhizosphere fungal communities vary by sediment type and dominant plant species cover in Nova Scotia, Canada.

Environ Microbiol Rep 2021 Aug 23;13(4):458-463. Epub 2020 Nov 23.

Department of Biology, Acadia University, Wolfville, Nova Scotia, Canada.

We surveyed Spartina saltmarsh sediment rhizosphere fungal communities at three saltmarshes and two timepoints in coastal Nova Scotia. Based on ITS2 Illumina miSeq rDNA data and multivariate analysis, neither sediment zone nor collection period correlated with fungal ASV richness, but collection site did. However, Shannon diversity indicated that sediment zone played a significant role in fungal diversity. For unweighted and weighted UniFrac distance, site was the major factor driving beta-diversity, with sediment zone and collection period having smaller roles. Sediment type and saltmarsh plant species may play important roles in structuring rhizosphere fungal assemblages, here dominated by ascomycetes. To our knowledge, our study is the first to assess fungal sediment communities in saltmarshes in Atlantic Canada using metabarcoding. It provides a biodiversity analysis of sediment fungi in a poorly studied but highly important ecosystem and points to their roles in nutrient cycling, blue carbon, coastal stability and coastal restoration. Our work will inform ongoing saltmarsh restoration in Atlantic Canada.
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http://dx.doi.org/10.1111/1758-2229.12904DOI Listing
August 2021

Tasting improvement in fruit flavor using genomics.

Authors:
Zoë Migicovsky

New Phytol 2020 06 28;226(6):1539-1540. Epub 2020 Apr 28.

Department of Plant, Food, and Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, B2N 5E3, Canada.

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http://dx.doi.org/10.1111/nph.16591DOI Listing
June 2020

Genome-wide association studies in apple reveal loci of large effect controlling apple polyphenols.

Hortic Res 2019 7;6:107. Epub 2019 Sep 7.

1Department of Plant and Animal Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS B2N 5E3 Canada.

Apples are a nutritious food source with significant amounts of polyphenols that contribute to human health and wellbeing, primarily as dietary antioxidants. Although numerous pre- and post-harvest factors can affect the composition of polyphenols in apples, genetics is presumed to play a major role because polyphenol concentration varies dramatically among apple cultivars. Here we investigated the genetic architecture of apple polyphenols by combining high performance liquid chromatography (HPLC) data with ~100,000 single nucleotide polymorphisms (SNPs) from two diverse apple populations. We found that polyphenols can vary in concentration by up to two orders of magnitude across cultivars, and that this dramatic variation was often predictable using genetic markers and frequently controlled by a small number of large effect genetic loci. Using GWAS, we identified candidate genes for the production of quercitrin, epicatechin, catechin, chlorogenic acid, 4--caffeoylquinic acid and procyanidins B1, B2, and C1. Our observation that a relatively simple genetic architecture underlies the dramatic variation of key polyphenols in apples suggests that breeders may be able to improve the nutritional value of apples through marker-assisted breeding or gene editing.
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http://dx.doi.org/10.1038/s41438-019-0190-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6804656PMC
September 2019

Genome-Wide Association Studies in Apple Reveal Loci for Aroma Volatiles, Sugar Composition, and Harvest Date.

Plant Genome 2019 06;12(2)

Understanding the genetic architecture of fruit quality traits is crucial to target breeding of apple ( L.) cultivars. We linked genotype and phenotype information by combining genotyping-by-sequencing (GBS) generated single nucleotide polymorphism (SNP) markers with fruit flavor volatile data, sugar and acid content, and historical trait data from a gene bank collection. Using gas chromatography-mass spectrometry (GC-MS) analysis of apple juice samples, we identified 49 fruit volatile organic compounds (VOCs). We found a very variable content of VOCs, especially for the esters, among 149 apple cultivars. We identified convincing associations for the acetate esters especially butyl acetate and hexyl acetate on chromosome 2 in a region of several alcohol acyl-transferases including AAT1. For sucrose content and for fructose and sucrose in percentage of total sugars, we revealed significant SNP associations. Here, we suggest a vacuolar invertase close to significant SNPs for this association as candidate gene. Harvest date was in strong SNP association with a NAC transcription factor gene and sequencing identified two haplotypes associated with harvest date. The study shows that SNP marker characterization of a gene bank collection can be successfully combined with new and historical trait data for association studies. Suggested candidate genes may contribute to an improved understanding of the genetic basis for important traits and simultaneously provide tools for targeted breeding using marker-assisted selection (MAS).
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http://dx.doi.org/10.3835/plantgenome2018.12.0104DOI Listing
June 2019

Rootstock effects on scion phenotypes in a 'Chambourcin' experimental vineyard.

Hortic Res 2019 1;6:64. Epub 2019 May 1.

2Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103-2010 USA.

Understanding how root systems modulate shoot system phenotypes is a fundamental question in plant biology and will be useful in developing resilient agricultural crops. Grafting is a common horticultural practice that joins the roots (rootstock) of one plant to the shoot (scion) of another, providing an excellent method for investigating how these two organ systems affect each other. In this study, we used the French-American hybrid grapevine 'Chambourcin' ( L.) as a model to explore the rootstock-scion relationship. We examined leaf shape, ion concentrations, and gene expression in 'Chambourcin' grown ungrafted as well as grafted to three different rootstocks ('SO4', '1103P' and '3309C') across 2 years and three different irrigation treatments. We found that a significant amount of the variation in leaf shape could be explained by the interaction between rootstock and irrigation. For ion concentrations, the primary source of variation identified was the position of a leaf in a shoot, although rootstock and rootstock by irrigation interaction also explained a significant amount of variation for most ions. Lastly, we found rootstock-specific patterns of gene expression in grafted plants when compared to ungrafted vines. Thus, our work reveals the subtle and complex effect of grafting on 'Chambourcin' leaf morphology, ionomics, and gene expression.
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http://dx.doi.org/10.1038/s41438-019-0146-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6491602PMC
May 2019

Apple whole genome sequences: recent advances and new prospects.

Hortic Res 2019 5;6:59. Epub 2019 Apr 5.

1Department of Horticulture, Washington State University, Pullman, WA 99164 USA.

In 2010, a major scientific milestone was achieved for tree fruit crops: publication of the first draft whole genome sequence (WGS) for apple (). This WGS, v1.0, was valuable as the initial reference for sequence information, fine mapping, gene discovery, variant discovery, and tool development. A new, high quality apple WGS, GDDH13 v1.1, was released in 2017 and now serves as the reference genome for apple. Over the past decade, these apple WGSs have had an enormous impact on our understanding of apple biological functioning, trait physiology and inheritance, leading to practical applications for improving this highly valued crop. Causal gene identities for phenotypes of fundamental and practical interest can today be discovered much more rapidly. Genome-wide polymorphisms at high genetic resolution are screened efficiently over hundreds to thousands of individuals with new insights into genetic relationships and pedigrees. High-density genetic maps are constructed efficiently and quantitative trait loci for valuable traits are readily associated with positional candidate genes and/or converted into diagnostic tests for breeders. We understand the species, geographical, and genomic origins of domesticated apple more precisely, as well as its relationship to wild relatives. The WGS has turbo-charged application of these classical research steps to crop improvement and drives innovative methods to achieve more durable, environmentally sound, productive, and consumer-desirable apple production. This review includes examples of basic and practical breakthroughs and challenges in using the apple WGSs. Recommendations for "what's next" focus on necessary upgrades to the genome sequence data pool, as well as for use of the data, to reach new frontiers in genomics-based scientific understanding of apple.
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http://dx.doi.org/10.1038/s41438-019-0141-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6450873PMC
April 2019

Population structure, relatedness and ploidy levels in an apple gene bank revealed through genotyping-by-sequencing.

PLoS One 2018 15;13(8):e0201889. Epub 2018 Aug 15.

Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg C, Denmark.

In recent years, new genome-wide marker systems have provided highly informative alternatives to low density marker systems for evaluating plant populations. To date, most apple germplasm collections have been genotyped using low-density markers such as simple sequence repeats (SSRs), whereas only a few have been explored using high-density genome-wide marker information. We explored the genetic diversity of the Pometum gene bank collection (University of Copenhagen, Denmark) of 349 apple accessions using over 15,000 genome-wide single nucleotide polymorphisms (SNPs) and 15 SSR markers, in order to compare the strength of the two approaches for describing population structure. We found that 119 accessions shared a putative clonal relationship with at least one other accession in the collection, resulting in the identification of 272 (78%) unique accessions. Of these unique accessions, over half (52%) share a first-degree relationship with at least one other accession. There is therefore a high degree of clonal and family relatedness in the Danish apple gene bank. We find significant genetic differentiation between Malus domestica and its supposed primary wild ancestor, M. sieversii, as well as between accessions of Danish origin and all others. Using the GBS approach allowed us to estimate ploidy levels, which were in accordance with flow cytometry results. Overall, we found strong concordance between analyses based on the genome-wide SNPs and the 15 SSR loci. However, we argue that GBS is superior to traditional SSR approaches because it allows detection of a much more detailed population structure and can be further exploited in genome-wide association studies (GWAS). Finally, we compare GBS with SSR for the purpose of identifying clones and pedigree relations in a diverse apple gene bank and discuss the advantages and constraints of the two approaches.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0201889PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6093671PMC
February 2019

Topological Data Analysis as a Morphometric Method: Using Persistent Homology to Demarcate a Leaf Morphospace.

Front Plant Sci 2018 25;9:553. Epub 2018 Apr 25.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, United States.

Current morphometric methods that comprehensively measure shape cannot compare the disparate leaf shapes found in seed plants and are sensitive to processing artifacts. We explore the use of persistent homology, a topological method applied as a filtration across simplicial complexes (or more simply, a method to measure topological features of spaces across different spatial resolutions), to overcome these limitations. The described method isolates subsets of shape features and measures the spatial relationship of neighboring pixel densities in a shape. We apply the method to the analysis of 182,707 leaves, both published and unpublished, representing 141 plant families collected from 75 sites throughout the world. By measuring leaves from throughout the seed plants using persistent homology, a defined morphospace comparing all leaves is demarcated. Clear differences in shape between major phylogenetic groups are detected and estimates of leaf shape diversity within plant families are made. The approach predicts plant family above chance. The application of a persistent homology method, using topological features, to measure leaf shape allows for a unified morphometric framework to measure plant form, including shapes, textures, patterns, and branching architectures.
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http://dx.doi.org/10.3389/fpls.2018.00553DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5996898PMC
April 2018

Prediction of Cacao () Resistance to spp. Diseases via Genome-Wide Association Analysis and Genomic Selection.

Front Plant Sci 2018 20;9:343. Epub 2018 Mar 20.

MARS, Incorporated c/o United States Department of Agriculture - Agricultural Research Service, Miami, FL, United States.

Cacao () is a globally important crop, and its yield is severely restricted by disease. Two of the most damaging diseases, witches' broom disease (WBD) and frosty pod rot disease (FPRD), are caused by a pair of related fungi: and , respectively. Resistant cultivars are the most effective long-term strategy to address diseases, but efficiently generating resistant and productive new cultivars will require robust methods for screening germplasm before field testing. Marker-assisted selection (MAS) and genomic selection (GS) provide two potential avenues for predicting the performance of new genotypes, potentially increasing the selection gain per unit time. To test the effectiveness of these two approaches, we performed a genome-wide association study (GWAS) and GS on three related populations of cacao in Ecuador genotyped with a 15K single nucleotide polymorphism (SNP) microarray for three measures of WBD infection (vegetative broom, cushion broom, and chirimoya pod), one of FPRD (monilia pod) and two productivity traits (total fresh weight of pods and % healthy pods produced). GWAS yielded several SNPs associated with disease resistance in each population, but none were significantly correlated with the same trait in other populations. Genomic selection, using one population as a training set to estimate the phenotypes of the remaining two (composed of different families), varied among traits, from a mean prediction accuracy of 0.46 (vegetative broom) to 0.15 (monilia pod), and varied between training populations. Simulations demonstrated that selecting seedlings using GWAS markers alone generates no improvement over selecting at random, but that GS improves the selection process significantly. Our results suggest that the GWAS markers discovered here are not sufficiently predictive across diverse germplasm to be useful for MAS, but that using all markers in a GS framework holds substantial promise in accelerating disease-resistance in cacao.
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http://dx.doi.org/10.3389/fpls.2018.00343DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5890178PMC
March 2018

Morphometrics Reveals Complex and Heritable Apple Leaf Shapes.

Front Plant Sci 2017 4;8:2185. Epub 2018 Jan 4.

Department of Plant, Food and Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada.

Apple ( spp.) is a widely grown and valuable fruit crop. Leaf shape is important for flowering in apple and may also be an early indicator for other agriculturally valuable traits. We examined 9,000 leaves from 869 unique apple accessions using linear measurements and comprehensive morphometric techniques. We identified allometric variation as the result of differing length-to-width aspect ratios between accessions and species of apple. The allometric variation was due to variation in the width of the leaf blade, not the length. Aspect ratio was highly correlated with the first principal component (PC1) of morphometric variation quantified using elliptical Fourier descriptors (EFDs) and persistent homology (PH). While the primary source of variation was aspect ratio, subsequent PCs corresponded to complex shape variation not captured by linear measurements. After linking the morphometric information with over 122,000 genome-wide single nucleotide polymorphisms (SNPs), we found high SNP heritability values even at later PCs, indicating that comprehensive morphometrics can capture complex, heritable phenotypes. Thus, techniques such as EFDs and PH are capturing heritable biological variation that would be missed using linear measurements alone.
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http://dx.doi.org/10.3389/fpls.2017.02185DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5758599PMC
January 2018

Patterns of genomic and phenomic diversity in wine and table grapes.

Hortic Res 2017 2;4:17035. Epub 2017 Aug 2.

Department of Plant, Food and Environmental Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS B2N 5E3, Canada.

Grapes are one of the most economically and culturally important crops worldwide, and they have been bred for both winemaking and fresh consumption. Here we evaluate patterns of diversity across 33 phenotypes collected over a 17-year period from 580 table and wine grape accessions that belong to one of the world's largest grape gene banks, the grape germplasm collection of the United States Department of Agriculture. We find that phenological events throughout the growing season are correlated, and quantify the marked difference in size between table and wine grapes. By pairing publicly available historical phenotype data with genome-wide polymorphism data, we identify large effect loci controlling traits that have been targeted during domestication and breeding, including hermaphroditism, lighter skin pigmentation and muscat aroma. Breeding for larger berries in table grapes was traditionally concentrated in geographic regions where Islam predominates and alcohol was prohibited, whereas wine grapes retained the ancestral smaller size that is more desirable for winemaking in predominantly Christian regions. We uncover a novel locus with a suggestive association with berry size that harbors a signature of positive selection for larger berries. Our results suggest that religious rules concerning alcohol consumption have had a marked impact on patterns of phenomic and genomic diversity in grapes.
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http://dx.doi.org/10.1038/hortres.2017.35DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5539807PMC
August 2017

LinkImputeR: user-guided genotype calling and imputation for non-model organisms.

BMC Genomics 2017 07 10;18(1):523. Epub 2017 Jul 10.

Department of Plant and Animal Sciences, Faculty of Agriculture, Dalhousie University, Truro, Nova Scotia, Canada.

Background: Genomic studies such as genome-wide association and genomic selection require genome-wide genotype data. All existing technologies used to create these data result in missing genotypes, which are often then inferred using genotype imputation software. However, existing imputation methods most often make use only of genotypes that are successfully inferred after having passed a certain read depth threshold. Because of this, any read information for genotypes that did not pass the threshold, and were thus set to missing, is ignored. Most genomic studies also choose read depth thresholds and quality filters without investigating their effects on the size and quality of the resulting genotype data. Moreover, almost all genotype imputation methods require ordered markers and are therefore of limited utility in non-model organisms.

Results: Here we introduce LinkImputeR, a software program that exploits the read count information that is normally ignored, and makes use of all available DNA sequence information for the purposes of genotype calling and imputation. It is specifically designed for non-model organisms since it requires neither ordered markers nor a reference panel of genotypes. Using next-generation DNA sequence (NGS) data from apple, cannabis and grape, we quantify the effect of varying read count and missingness thresholds on the quantity and quality of genotypes generated from LinkImputeR. We demonstrate that LinkImputeR can increase the number of genotype calls by more than an order of magnitude, can improve genotyping accuracy by several percent and can thus improve the power of downstream analyses. Moreover, we show that the effects of quality and read depth filters can differ substantially between data sets and should therefore be investigated on a per-study basis.

Conclusions: By exploiting DNA sequence data that is normally ignored during genotype calling and imputation, LinkImputeR can significantly improve both the quantity and quality of genotype data generated from NGS technologies. It enables the user to quickly and easily examine the effects of varying thresholds and filters on the number and quality of the resulting genotype calls. In this manner, users can decide on thresholds that are most suitable for their purposes. We show that LinkImputeR can significantly augment the value and utility of NGS data sets, especially in non-model organisms with poor genomic resources.
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http://dx.doi.org/10.1186/s12864-017-3873-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5504746PMC
July 2017

Exploiting Wild Relatives for Genomics-assisted Breeding of Perennial Crops.

Front Plant Sci 2017 4;8:460. Epub 2017 Apr 4.

Department of Plant, Food and Environmental Sciences, Faculty of Agriculture, Dalhousie University,Truro, NS, Canada.

Perennial crops are vital contributors to global food production and nutrition. However, the breeding of new perennial crops is an expensive and time-consuming process due to the large size and lengthy juvenile phase of many species. Genomics provides a valuable tool for improving the efficiency of breeding by allowing progeny possessing a trait of interest to be selected at the seed or seedling stage through marker-assisted selection (MAS). The benefits of MAS to a breeder are greatest when the targeted species takes a long time to reach maturity and is expensive to grow and maintain. Thus, MAS holds particular promise in perennials since they are often costly and time-consuming to grow to maturity and evaluate. Well-characterized germplasm that breeders can tap into for improving perennials is often limited in genetic diversity. Wild relatives are a largely untapped source of desirable traits including disease resistance, fruit quality, and rootstock characteristics. This review focuses on the use of genomics-assisted breeding in perennials, especially as it relates to the introgression of useful traits from wild relatives. The identification of genetic markers predictive of beneficial phenotypes derived from wild relatives is hampered by genomic tools designed for domesticated species that are often ill-suited for use in wild relatives. There is therefore an urgent need for better genomic resources from wild relatives. A further barrier to exploiting wild diversity through genomics is the phenotyping bottleneck: well-powered genetic mapping requires accurate and cost-effective characterization of large collections of diverse wild germplasm. While genomics will always be used in combination with traditional breeding methods, it is a powerful tool for accelerating the speed and reducing the costs of breeding while harvesting the potential of wild relatives for improving perennial crops.
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http://dx.doi.org/10.3389/fpls.2017.00460DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5379136PMC
April 2017

Genome to Phenome Mapping in Apple Using Historical Data.

Plant Genome 2016 07;9(2)

Apple ( X Borkh.) is one of the world's most valuable fruit crops. Its large size and long juvenile phase make it a particularly promising candidate for marker-assisted selection (MAS). However, advances in MAS in apple have been limited by a lack of phenotype and genotype data from sufficiently large samples. To establish genotype-phenotype relationships and advance MAS in apple, we extracted over 24,000 phenotype scores from the USDA-Germplasm Resources Information Network (GRIN) database and linked them with over 8000 single nucleotide polymorphisms (SNPs) from 689 apple accessions from the USDA apple germplasm collection clonally preserved in Geneva, NY. We find significant genetic differentiation between Old World and New World cultivars and demonstrate that the genetic structure of the domesticated apple also reflects the time required for ripening. A genome-wide association study (GWAS) of 36 phenotypes confirms the association between fruit color and the MYB1 locus, and we also report a novel association between the transcription factor, NAC18.1, and harvest date and fruit firmness. We demonstrate that harvest time and fruit size can be predicted with relatively high accuracies ( > 0.46) using genomic prediction. Rapid decay of linkage disequilibrium (LD) in apples means millions of SNPs may be required for well-powered GWAS. However, rapid LD decay also promises to enable extremely high resolution mapping of causal variants, which holds great potential for advancing MAS.
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http://dx.doi.org/10.3835/plantgenome2015.11.0113DOI Listing
July 2016

Genomic ancestry estimation quantifies use of wild species in grape breeding.

BMC Genomics 2016 06 30;17:478. Epub 2016 Jun 30.

Department of Plant and Animal Sciences, Faculty of Agriculture, Dalhousie University, Truro, NS, Canada.

Background: Grapes are one of the world's most valuable crops and most are made into wine. Grapes belong to the genus Vitis, which includes over 60 inter-fertile species. The most common grape cultivars derive their entire ancestry from the species Vitis vinifera, but wild relatives have also been exploited to create hybrid cultivars, often with increased disease resistance.

Results: We evaluate the genetic ancestry of some of the most widely grown commercial hybrids from North America and Europe. Using genotyping-by-sequencing (GBS), we generated 2482 SNPs and 56 indels from 7 wild Vitis, 7 V. vinifera, and 64 hybrid cultivars. We used a principal component analysis (PCA) based ancestry estimation procedure and verified its accuracy with both empirical and simulated data. V. vinifera ancestry ranged from 11 % to 76 % across hybrids studied. Approximately one third (22/64) of the hybrids have ancestry estimates consistent with F1 hybridization: they derive half of their ancestry from wild Vitis and half from V. vinifera.

Conclusions: Our results suggest that hybrid grape breeding is in its infancy. The distribution of V. vinifera ancestry across hybrids also suggests that backcrosses to wild Vitis species have been more frequent than backcrosses to V. vinifera during hybrid grape breeding. This pattern is unusual in crop breeding, as it is most common to repeatedly backcross to elite, or domesticated, germplasm. We anticipate our method can be extended to facilitate marker-assisted selection in order to introgress beneficial wild Vitis traits, while allowing for offspring with the highest V. vinifera content to be selected at the seedling stage.
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http://dx.doi.org/10.1186/s12864-016-2834-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4928267PMC
June 2016

LinkImpute: Fast and Accurate Genotype Imputation for Nonmodel Organisms.

G3 (Bethesda) 2015 Sep 15;5(11):2383-90. Epub 2015 Sep 15.

Department of Plant and Animal Sciences, Faculty of Agriculture, Dalhousie University, Truro, Nova Scotia, B2N 5E3, Canada.

Obtaining genome-wide genotype data from a set of individuals is the first step in many genomic studies, including genome-wide association and genomic selection. All genotyping methods suffer from some level of missing data, and genotype imputation can be used to fill in the missing data and improve the power of downstream analyses. Model organisms like human and cattle benefit from high-quality reference genomes and panels of reference genotypes that aid in imputation accuracy. In nonmodel organisms, however, genetic and physical maps often are either of poor quality or are completely absent, and there are no panels of reference genotypes available. There is therefore a need for imputation methods designed specifically for nonmodel organisms in which genomic resources are poorly developed and marker order is unreliable or unknown. Here we introduce LinkImpute, a software package based on a k-nearest neighbor genotype imputation method, LD-kNNi, which is designed for unordered markers. No physical or genetic maps are required, and it is designed to work on unphased genotype data from heterozygous species. It exploits the fact that markers useful for imputation often are not physically close to the missing genotype but rather distributed throughout the genome. Using genotyping-by-sequencing data from diverse and heterozygous accessions of apples, grapes, and maize, we compare LD-kNNi with several genotype imputation methods and show that LD-kNNi is fast, comparable in accuracy to the best-existing methods, and exhibits the least bias in allele frequency estimates.
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http://dx.doi.org/10.1534/g3.115.021667DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4632058PMC
September 2015

Transgenerational changes in plant physiology and in transposon expression in response to UV-C stress in Arabidopsis thaliana.

Plant Signal Behav 2014 ;9(11):e976490

a Department of Biological Sciences ; University of Lethbridge ; Lethbridge , AB , Canada.

Stress has a negative impact on crop yield by altering a gain in biomass and affecting seed set. Recent reports suggest that exposure to stress also influences the response of the progeny. In this paper, we analyzed seed size, leaf size, bolting time and transposon expression in 2 consecutive generations of Arabidopsis thaliana plants exposed to moderate UV-C stress. Since previous reports suggested a potential role of Dicer-like (DCL) proteins in the establishment of transgenerational response, we used dcl2, dcl3 and dcl4 mutants in parallel with wild-type plants. These studies revealed that leaf number decreased in the progeny of UV-C stressed plants, and bolting occurred later. Transposons were also re-activated in the progeny of stressed plants. Changes in the dcl mutants were less prominent than in wild-type plants. DCL2 and DCL3 appeared to be more important in the transgenerational stress memory than DCL4 because transgenerational changes were less profound in the dcl2 and dcl3 mutants.
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http://dx.doi.org/10.4161/15592324.2014.976490DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4622705PMC
September 2015

Transgenerational phenotypic and epigenetic changes in response to heat stress in Arabidopsis thaliana.

Plant Signal Behav 2014 10;9(2):e27971. Epub 2014 Feb 10.

Department of Biological Sciences, University of Lethbridge, Lethbridge, AB Canada.

Exposure to heat stress causes physiological and epigenetic changes in plants, which may also be altered in the progeny. We compared the progeny of stressed and control Arabidopsis thaliana wild type and Dicer-like mutant dcl2, dcl3, and dcl4 plants for variations in physiology and molecular profile, including global genome methylation, mRNA levels, and histone modifications in the subset of differentially expressed genes at normal conditions and in response to heat stress. We found that the immediate progeny of heat-stressed plants had fewer, but larger leaves, and tended to bolt earlier. Transposon expression was elevated in the progeny of heat-stressed plants, and heat stress in the same generation tended to decrease global genome methylation. Progeny of stressed plants had increased expression of HSFA2, and reduction in MSH2, ROS1, and several SUVH genes. Gene expression positively correlated with permissive histone marks and negatively correlated with repressive marks. Overall, the progeny of heat stressed plants varied in both their physiology and epigenome and dcl2 and dcl3 mutants were partially deficient for these changes.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4091214PMC
http://dx.doi.org/10.4161/psb.27971DOI Listing
June 2015

Changes to DNA methylation and homologous recombination frequency in the progeny of stressed plants.

Biochem Cell Biol 2013 Feb 31;91(1):1-5. Epub 2013 Jan 31.

University of Lethbridge, Department of Biological Sciences, Lethbridge, AB T1K 3M4, Canada.

Plants undergo changes in response to biotic and abiotic stresses that help them adjust and survive. Some of these changes may even be passed on to progeny and eventually lead to adaptive evolution. Transgenerational changes in response to stress include alterations in DNA methylation and changes in homologous recombination frequency (HRF). The progeny of plants that were stressed often show elevated HRF as well as genomic hypermethylation, although specific loci that are beneficial in times of stress may be hypomethylated. One of the possible mechanisms responsible for passing the memory to the progeny involves small interfering RNAs; Dicer-like proteins, DCL2 and DCL3, are in part required for this process. However, while epigenetic modifications are often present in the untreated progeny of stressed plants, they are not usually sustained for multiple unexposed generations. Still, transgenerational inheritance of such changes has already begun to provide evidence for an important role of epigenetics in enhancing stress resistance.
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http://dx.doi.org/10.1139/bcb-2012-0046DOI Listing
February 2013

Epigenetic Modifications during Angiosperm Gametogenesis.

Front Plant Sci 2012 6;3:20. Epub 2012 Feb 6.

Department of Biological Sciences, University of Lethbridge Lethbridge, AB, Canada.

Angiosperms do not contain a distinct germline, but rather develop gametes from gametophyte initials that undergo cell division. These gametes contain cells that give rise to an endosperm and the embryo. DNA methylation is decreased in the vegetative nucleus (VN) and central cell nuclei (CCN) resulting in expression of transposable elements (TEs). It is thought that the siRNAs produced in response to TE expression are able to travel to the sperm cells and egg cells (EC) from VN and CCN, respectively, in order to enforce silencing there. Demethylation during gametogenesis helps ensure that even newly integrated TEs are expressed and therefore silenced by the resulting siRNA production. A final form of epigenetic control is modification of histones, which includes accumulation of the H3 variant HTR10 in mature sperm that is then completely replaced following fertilization. In females, the histone isoforms present in the EC and CCN differ, potentially helping to differentiate the two components during gametogenesis.
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http://dx.doi.org/10.3389/fpls.2012.00020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3355800PMC
August 2012

Epigenetic memory in mammals.

Front Genet 2011 8;2:28. Epub 2011 Jun 8.

Department of Biological Sciences, University of Lethbridge Lethbridge, AB, Canada.

Epigenetic information can be passed on from one generation to another via DNA methylation, histone modifications, and changes in small RNAs, a process called epigenetic memory. During a mammal's lifecycle epigenetic reprogramming, or the resetting of most epigenetic marks, occurs twice. The first instance of reprogramming occurs in primordial germ cells and the second occurs following fertilization. These processes may be both passive and active. In order for epigenetic inheritance to occur the epigenetic modifications must be able to escape reprogramming. There are several examples supporting this non-Mendelian mechanism of inheritance including the prepacking of early developmental genes in histones instead of protamines in sperm, genomic imprinting via methylation marks, the retention of CenH3 in mammalian sperm and the inheritance of piwi-associated interfering RNAs. The ability of mammals to pass on epigenetic information to their progeny provides clear evidence that inheritance is not restricted to DNA sequence and epigenetics plays a key role in producing viable offspring.
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http://dx.doi.org/10.3389/fgene.2011.00028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3268583PMC
October 2012

Transgenerational adaptation to heavy metal salts in Arabidopsis.

Front Plant Sci 2011 5;2:91. Epub 2011 Dec 5.

Department of Biological Sciences, University of Lethbridge Lethbridge, AB, Canada.

Exposure to abiotic and biotic stress results in changes in plant physiology and triggers genomic instability. Recent reports suggest that the progeny of stressed plants also exhibit changes in genome stability, stress tolerance, and methylation. Here we analyzed whether exposure to Ni(2+), Cd(2+), and Cu(2+) salts leads to transgenerational changes in homologous recombination frequency and stress tolerance. We found that the immediate progeny of stressed plants exhibited an increased rate of recombination. However, when the progeny of stressed plants was propagated without stress, recombination reverted to normal levels. Exposure of plants to heavy metals for five consecutive generations (S1-S5) resulted in recombination frequency being maintained at a high level. Skipping stress following two to three generations of propagation with 50 mM Ni(2+) or Cd(2+) did not decrease the recombination frequency, suggesting plant acclimation to upregulated recombination. Analysis of the progeny of plants exposed to Cu(2+) and Ni(2+) indicated higher stress tolerance to the heavy metal parental plants were exposed to. Tolerance was higher in plants propagated with stress for three to five generations, which resulted in longer roots than plants propagated on heavy metals for only one to two generations. Tolerance was also more prominent upon exposure to a higher concentration of salts. The progeny of stressed plants were also more tolerant to NaCl and methyl methane sulfonate.
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http://dx.doi.org/10.3389/fpls.2011.00091DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3355606PMC
August 2012
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