Publications by authors named "Jason Londo"

32 Publications

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

A key 'foxy' aroma gene is regulated by homology-induced promoter indels in the iconic juice grape 'Concord'.

Hortic Res 2020 Apr 18;7(1):67. Epub 2020 Apr 18.

US Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY, USA.

'Concord', the most well-known juice grape with a parentage of the North American grape species Vitis labrusca L., possesses a special 'foxy' aroma predominantly resulted from the accumulation of methyl anthranilate (MA) in berries. This aroma, however, is often perceived as an undesirable attribute by wine consumers and rarely noticeable in the common table and wine grape species V. vinifera. Here we discovered homology-induced promoter indels as a major genetic mechanism for species-specific regulation of a key 'foxy' aroma gene, anthraniloyl-CoA:methanol acyltransferase (AMAT), that is responsible for MA biosynthesis. We found the absence of a 426-bp and/or a 42-bp sequence in AMAT promoters highly associated with high levels of AMAT expression and MA accumulation in 'Concord' and other V. labrusca-derived grapes. These promoter variants, all with direct and inverted repeats, were further confirmed in more than 1,300 Vitis germplasm. Moreover, functional impact of these indels was validated in transgenic Arabidopsis. Superimposed on the promoter regulation, large structural changes including exonic insertion of a retrotransposon were present at the AMAT locus in some V. vinifera grapes. Elucidation of the AMAT genetic regulation advances our understanding of the 'foxy' aroma trait and makes it genetically trackable and amenable in grapevine breeding.
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http://dx.doi.org/10.1038/s41438-020-0304-6DOI Listing
April 2020

Multiple independent recombinations led to hermaphroditism in grapevine.

Proc Natl Acad Sci U S A 2021 Apr;118(15)

Horticulture Section, School of Integrative Plant Science, Cornell AgriTech, Cornell University, Geneva, NY 14456;

Hermaphroditic (perfect) flowers were a key trait in grapevine domestication, enabling a drastic increase in yields due to the efficiency of self-pollination in the domesticated grapevine ( L. ssp. ). In contrast, all extant wild species are dioecious, each plant having only male or female flowers. In this study, we identified the male (M) and female (f) haplotypes of the sex-determining region (SDR) in the wild grapevine species and confirmed the boundaries of the SDR. We also demonstrated that the SDR and its boundaries are precisely conserved across the genus using shotgun resequencing data of 556 wild and domesticated accessions from North America, East Asia, and Europe. A high linkage disequilibrium was found at the SDR in all wild grape species, while different recombination signatures were observed along the hermaphrodite (H) haplotype of 363 cultivated accessions, revealing two distinct H haplotypes, named H1 and H2. To further examine the H2 haplotype, we sequenced the genome of two grapevine cultivars, 'Riesling' and 'Chardonnay'. By reconstructing the first two H2 haplotypes, we estimated the divergence time between H1 and H2 haplotypes at ∼6 million years ago, which predates the domestication of grapevine (∼8,000 y ago). Our findings emphasize the important role of recombination suppression in maintaining dioecy in wild grape species and lend additional support to the hypothesis that at least two independent recombination events led to the reversion to hermaphroditism in grapevine.
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http://dx.doi.org/10.1073/pnas.2023548118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8053984PMC
April 2021

Identification of SNPs associated with magnesium and sodium uptake and the effect of their accumulation on micro and macro nutrient levels in .

PeerJ 2021 8;9:e10773. Epub 2021 Feb 8.

E&J Gallo Winery, Modesto, CA, United States of America.

Macro and micro nutrient accumulation affects all stages of plant growth and development. When nutrient deficiencies or excesses occur, normal plant growth is altered resulting in symptoms such as leaf chlorosis, plant stunting or death. In grapes, few genomic regions associated with nutrient accumulation or deficiencies have been identified. Our study evaluated micro and macro nutrient concentrations in L. to identify associated SNPs using an association approach with genotype by sequencing data. Nutrient concentrations and foliar symptoms (leaf chlorosis and stunting) were compared among 249 F individuals in 2015 and 2016. Foliar symptoms were consistent (≥90%) between years and correlated with changes in nutrient concentrations of magnesium ( = 0.65 and  = 0.38 in 2015 and 2016, respectively), aluminum ( = 0.24 and  = 0.49), iron ( = 0.21 and  = 0.49), and sodium ( = 0.32 and  = 0.21). Single nucleotide polymorphisms associated with symptoms, sodium, and magnesium were detected on each chromosome with the exception of 5, 7 and 17 depending on the trait and genome used for analyses explaining up to 40% of the observed variation. Symptoms and magnesium concentration were primarily associated with SNPs on chromosome 3, while SNPs associated with increased sodium content were primarily found on chromosomes 11 and 18. Mean concentrations for each nutrient varied between years in the population between symptomatic and asymptomatic plants, but relative relationships were mostly consistent. These data suggest a complex relationship among foliar symptoms and micro and macro nutrients accumulating in grapevines.
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http://dx.doi.org/10.7717/peerj.10773DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7877238PMC
February 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

Draft genome of the Native American cold hardy grapevine Michx. 'Manitoba 37'.

Hortic Res 2020 1;7(1):92. Epub 2020 Jun 1.

Agronomy, Horticulture and Plant Science Department and BioSNTR, South Dakota State University, Brookings, SD 57006 USA.

, a critically important Native American grapevine species, is used globally in rootstock and scion breeding and contributed to the recovery of the French wine industry during the mid-19th century phylloxera epidemic. This species has abiotic and biotic stress tolerance and the largest natural geographic distribution of the North American grapevine species. Here we report an Illumina short-read 369X coverage, draft de novo heterozygous genome sequence of Michx. 'Manitoba 37' with the size of ~495 Mb for 69,616 scaffolds and a N50 length of 518,740 bp. Using RNAseq data, 40,019 coding sequences were predicted and annotated. Benchmarking with Universal Single-Copy Orthologs (BUSCO) analysis of predicted gene models found 96% of the complete BUSCOs in this assembly. The assembly continuity and completeness were further validated using ESTs, BACs, and three de novo transcriptome assemblies of three different genotypes resulting in >98% of respective sequences/transcripts mapping with this assembly. Alignment of the assembly and predicted CDS with the latest 'PN40024' CDS and genome assembly showed 99% CDS alignment and a high degree of synteny. An analysis of plant transcription factors indicates a high degree of homology with the transcription factors. QTL mapping to 'Manitoba 37' and PN40024 has identified genetic relationships to phenotypic variation between species. This assembly provides reference sequences, gene models for marker development and understanding 's genetic contributions in grape breeding and research.
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http://dx.doi.org/10.1038/s41438-020-0316-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7261805PMC
June 2020

A key 'foxy' aroma gene is regulated by homology-induced promoter indels in the iconic juice grape 'Concord'.

Hortic Res 2020 18;7:67. Epub 2020 Apr 18.

1US Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY USA.

'Concord', the most well-known juice grape with a parentage of the North American grape species L., possesses a special 'foxy' aroma predominantly resulted from the accumulation of methyl anthranilate (MA) in berries. This aroma, however, is often perceived as an undesirable attribute by wine consumers and rarely noticeable in the common table and wine grape species . Here we discovered homology-induced promoter indels as a major genetic mechanism for species-specific regulation of a key 'foxy' aroma gene, anthraniloyl-CoA:methanol acyltransferase (), that is responsible for MA biosynthesis. We found the absence of a 426-bp and/or a 42-bp sequence in promoters highly associated with high levels of expression and MA accumulation in 'Concord' and other -derived grapes. These promoter variants, all with direct and inverted repeats, were further confirmed in more than 1,300 germplasm. Moreover, functional impact of these indels was validated in transgenic . Superimposed on the promoter regulation, large structural changes including exonic insertion of a retrotransposon were present at the locus in some grapes. Elucidation of the genetic regulation advances our understanding of the 'foxy' aroma trait and makes it genetically trackable and amenable in grapevine breeding.
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http://dx.doi.org/10.1038/s41438-020-0304-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7166211PMC
April 2020

Haplotyping the Vitis collinear core genome with rhAmpSeq improves marker transferability in a diverse genus.

Nat Commun 2020 01 21;11(1):413. Epub 2020 Jan 21.

USDA-ARS, Grape Genetics Research Unit, Geneva, NY, 14456, USA.

Transferable DNA markers are essential for breeding and genetics. Grapevine (Vitis) breeders utilize disease resistance alleles from congeneric species ~20 million years divergent, but existing Vitis marker platforms have cross-species transfer rates as low as 2%. Here, we apply a marker strategy targeting the inferred Vitis core genome. Incorporating seven linked-read de novo assemblies and three existing assemblies, the Vitis collinear core genome is estimated to converge at 39.8 Mb (8.67% of the genome). Adding shotgun genome sequences from 40 accessions enables identification of conserved core PCR primer binding sites flanking polymorphic haplotypes with high information content. From these target regions, we develop 2,000 rhAmpSeq markers as a PCR multiplex and validate the panel in four biparental populations spanning the diversity of the Vitis genus, showing transferability increases to 91.9%. This marker development strategy should be widely applicable for genetic studies in many taxa, particularly those ~20 million years divergent.
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http://dx.doi.org/10.1038/s41467-019-14280-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6972940PMC
January 2020

Quantitative Trait Locus Analysis of Leaf Morphology Indicates Conserved Shape Loci in Grapevine.

Front Plant Sci 2019 15;10:1373. Epub 2019 Nov 15.

Horticulture Section, School of Integrative Plant Science, Cornell Agritech at the New York State Agricultural Experiment Station, Geneva, NY, United States.

Leaf shape in plants plays important roles in water use, canopy structure, and physiological tolerances to abiotic stresses; all important traits for the future development and sustainability of grapevine cultivation. Historically, researchers have used ampelography, the study of leaf shape in grapevines, to differentiate species and cultivars based on finite leaf attributes. However, ampelographic measurements have limitations and new methods for quantifying shape are now available. We paired an analysis of finite trait attributes with a 17-point landmark survey and generalized Procrustes analysis (GPA) to reconstruct grapevine leaves digitally from five interspecific hybrid mapping families. Using the reconstructed leaves, we performed three types of quantitative trait loci (QTL) analyses to determine the genetic architecture that defines leaf shape. In the first analysis, we compared several important ampelographic measurements as finite trait QTL. In the second and third analyses, we identified significant shape variation principal components analysis (PCA) and using a multivariate least squares interval mapping (MLSIM) approach. In total, we identified 271 significant QTL across the three measures of leaf shape and identified specific QTL hotspots in the grape genome which appear to drive major aspects of grapevine leaf shape.
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http://dx.doi.org/10.3389/fpls.2019.01373DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6873345PMC
November 2019

X-ray phase contrast imaging of Vitis spp. buds shows freezing pattern and correlation between volume and cold hardiness.

Sci Rep 2019 10 18;9(1):14949. Epub 2019 Oct 18.

Cornell High Energy Synchrotron Source, Cornell University, Ithaca, NY, USA.

Grapevine (Vitis spp.) buds must survive winter temperatures in order to resume growth when suitable conditions return in spring. They do so by developing cold hardiness through deep supercooling, but the mechanistic process of supercooling in buds remains largely unknown. Here we use synchrotron X-ray phase contrast imaging to study cold hardiness-related characteristics of V. amurensis, V. riparia, and V. vinifera buds: time-resolved 2D imaging was used to visualize freezing; and microtomography was used to evaluate morphological changes during deacclimation. Bud cold hardiness was determined (low temperature exotherms; LTEs) using needle thermocouples during 2D imaging as buds were cooled with a N gas cryostream. Resolution in 2D imaging did not allow for ice crystal identification, but freezing was assessed by movement of tissues coinciding with LTE values. Freezing was observed to propagate from the center of the bud toward the outer bud scales. The freezing events observed lasted several minutes. Additionally, loss of supercooling ability appears to be correlated with increases in bud tissue volume during the process of deacclimation, but major increases in volume occur after most of the supercooling ability is lost, suggesting growth resumption processes are limited by deacclimation state.
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http://dx.doi.org/10.1038/s41598-019-51415-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6802181PMC
October 2019

Deacclimation kinetics as a quantitative phenotype for delineating the dormancy transition and thermal efficiency for budbreak in species.

AoB Plants 2018 Oct 11;10(5):ply066. Epub 2018 Oct 11.

School of Integrative Plant Science - Horticulture Section, Cornell University-New York State Agricultural Experiment Station, Geneva, NY, USA.

Bud dormancy and cold hardiness are critical adaptations for surviving winter cold stress for temperate perennial plant species. In grapevine, acquisition of cold hardiness requires dormancy induction in the early winter and careful maintenance of dormancy state throughout winter. With sufficient exposure to low, non-freezing temperatures (chilling requirement), grapevine buds transition between early (endodormant) and late winter (ecodormant) states. The objective of this study was to uncover the relationship between fulfilment of the chilling requirement and the effects of various temperatures on loss of cold hardiness (deacclimation). The relationship between chilling requirement and temperature as it affects the rate of deacclimation ( ) was examined for dormant cuttings of , , and . The effect of temperature on was exponential at low and logarithmic at high temperatures. Deacclimation rates also increased in magnitude as chilling accumulated demonstrating a change in deacclimation potential (Ψ), following a logarithmic response. The combination of Ψ and indicates genotype-specific thermal efficiency for deacclimation and growth in that may be overlooked by simple growing degree-day computations. The Ψ and parameters are genotype-specific and will greatly increase the refinement of models predicting effects of climate change on phenology. Deacclimation rates represent a quantitative determinant of dormancy transition and budbreak in grapevine and will assist researchers in selecting germplasm for differences in chilling requirement and thermal efficiency.
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http://dx.doi.org/10.1093/aobpla/ply066DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6207836PMC
October 2018

Characterizing 3D inflorescence architecture in grapevine using X-ray imaging and advanced morphometrics: implications for understanding cluster density.

J Exp Bot 2019 11;70(21):6261-6276

Donald Danforth Plant Science Center, St Louis, MO, USA.

Inflorescence architecture provides the scaffold on which flowers and fruits develop, and consequently is a primary trait under investigation in many crop systems. Yet the challenge remains to analyse these complex 3D branching structures with appropriate tools. High information content datasets are required to represent the actual structure and facilitate full analysis of both the geometric and the topological features relevant to phenotypic variation in order to clarify evolutionary and developmental inflorescence patterns. We combined advanced imaging (X-ray tomography) and computational approaches (topological and geometric data analysis and structural simulations) to comprehensively characterize grapevine inflorescence architecture (the rachis and all branches without berries) among 10 wild Vitis species. Clustering and correlation analyses revealed unexpected relationships, for example pedicel branch angles were largely independent of other traits. We identified multivariate traits that typified species, which allowed us to classify species with 78.3% accuracy, versus 10% by chance. Twelve traits had strong signals across phylogenetic clades, providing insight into the evolution of inflorescence architecture. We provide an advanced framework to quantify 3D inflorescence and other branched plant structures that can be used to tease apart subtle, heritable features for a better understanding of genetic and environmental effects on plant phenotypes.
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http://dx.doi.org/10.1093/jxb/erz394DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6859732PMC
November 2019

Tempo of gene regulation in wild and cultivated Vitis species shows coordination between cold deacclimation and budbreak.

Plant Sci 2019 Oct 25;287:110178. Epub 2019 Jun 25.

School of Integrative Plant Science - Horticulture Section, Cornell University - Cornell AgriTech, 15 Castle Creek Drive 630, Geneva, NY, USA; United States Department of Agriculture, Agricultural Research Service, Grape Genetics Research Unit, 15 Castle Creek Drive 630, Geneva, NY, USA. Electronic address:

Dormancy release, loss of cold hardiness and budbreak are critical aspects of the annual cycle of deciduous perennial plants. Molecular control of these processes is not fully understood, and genotypic variation may be important for climate adaptation. To gain greater understanding of these processes, single-node cuttings from wild (Vitis amurensis, V. riparia) and cultivated Vitis genotypes (V. vinifera 'Cabernet Sauvignon', 'Riesling') were collected from the vineyard during winter and placed under forcing conditions. Cold hardiness was measured daily, and buds were collected for gene expression analysis until budbreak. Wild Vitis genotypes had faster deacclimation and budbreak than V. vinifera. Temperature-sensing related genes were quickly and synchronously differentially expressed in all genotypes. Significant changes in the pattern of expression changes for eight major metabolic and hormone related pathways were seen across all genotypes. Downregulation of ABA synthesis appears to play an important role in loss of cold hardiness and budbreak in all genotypes. This role was validated through an observed halt in cold hardiness loss of 'Riesling' buds treated with exogenous ABA. The gene expression cascade that occurs during deacclimation and budbreak phenology of fast (wild) and slow (cultivated) grapevines appears coordinated and temporally conserved within these phenotypes.
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http://dx.doi.org/10.1016/j.plantsci.2019.110178DOI Listing
October 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

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

High-throughput sequencing data clarify evolutionary relationships among North American Vitis species and improve identification in USDA Vitis germplasm collections.

Am J Bot 2018 02 12;105(2):215-226. Epub 2018 Mar 12.

United States Department of Agriculture, Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY, 14425, USA.

Premise Of The Study: Grapes are one of the most economically important berry crops worldwide, with the vast majority of production derived from the domesticated Eurasian species Vitis vinifera. Expansion of production into new areas, development of new cultivars, and concerns about adapting grapevines for changing climates necessitate the use of wild grapevine species in breeding programs. Diversity within Vitis has long been a topic of study; however, questions remain regarding relationships between species. Furthermore, the identity of some living accessions is unclear.

Methods: This study generated 11,020 single nucleotide polymorphism (SNP) markers for more than 300 accessions in the USDA-ARS grape germplasm repository using genotyping-by-sequencing. Resulting data sets were used to reconstruct evolutionary relationships among several North American and Eurasian Vitis species, and to suggest taxonomic labels for previously unidentified and misidentified germplasm accessions based on genetic distance.

Key Results: Maximum likelihood analyses of SNP data support the monophyly of Vitis, subg. Vitis, a Eurasian subg. Vitis clade, and a North American subg. Vitis clade. Data delineate species groups within North America. In addition, analysis of genetic distance suggested taxonomic identities for 20 previously unidentified Vitis accessions and for 28 putatively misidentified accessions.

Conclusions: This work advances understanding of Vitis evolutionary relationships and provides the foundation for ongoing germplasm enhancement. It supports conservation and breeding efforts by contributing to a growing genetic framework for identifying novel genetic variation and for incorporating new, unsampled populations into the germplasm repository system.
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http://dx.doi.org/10.1002/ajb2.1033DOI Listing
February 2018

Divergence in the transcriptional landscape between low temperature and freeze shock in cultivated grapevine ().

Hortic Res 2018 1;5:10. Epub 2018 Mar 1.

1United States Department of Agriculture, Agricultural Research Service, Grape Genetics Research Unit, 630 W. North Street, Geneva, NY USA.

Low-temperature stresses limit the sustainability and productivity of grapevines when early spring frosts damage young grapevine leaves. Spring conditions often expose grapevines to low, but not damaging, chilling temperatures and these temperatures have been shown to increase freeze resistance in other model systems. In this study, we examined whole-transcriptome gene expression patterns of young leaf tissue from cuttings of five different grapevine cultivars, exposed to chill and freeze shock, in order to understand the underlying transcriptional landscape associated with cold stress response. No visible damage was observed when grapevine leaves were exposed to chilling temperatures while freeze temperatures resulted in variable damage in all cultivars. Significant differences in gene expression were observed between warm control conditions and all types of cold stress. Exposure to chill stress (4 °C) versus freezing stress (-3 °C) resulted in very different patterns of gene expression and enriched pathway responses. Genes from the ethylene signaling, ABA signaling, the AP2/ERF, WRKY, and NAC transcription factor families, and starch/sucrose/galactose pathways were among the most commonly observed to be differentially regulated. Preconditioning leaves to chill temperatures prior to freezing temperatures resulted in slight buffering of gene expression responses, suggesting that differences between chill and freeze shock perception complicates identification of candidate genes for cold resistance in grapevine. Overall, the transcriptional landscape contrasts observed between low temperature and freezing stresses demonstrate very different activation of candidate pathways impacting grapevine cold response.
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http://dx.doi.org/10.1038/s41438-018-0020-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5830407PMC
March 2018

RNA-seq-based genome annotation and identification of long-noncoding RNAs in the grapevine cultivar 'Riesling'.

BMC Genomics 2017 Dec 2;18(1):937. Epub 2017 Dec 2.

United States Department of Agriculture, Agricultural Research Service, Grape Genetics Research Unit, 630 W. North Street, Geneva, NY, USA.

Background: The technological advances of RNA-seq and de novo transcriptome assembly have enabled genome annotation and transcriptome profiling in highly heterozygous species such as grapevine (Vitis vinifera L.). This work is an attempt to utilize a de novo-assembled transcriptome of the V. vinifera cultivar 'Riesling' to improve annotation of the grapevine reference genome sequence.

Results: Here we show that the transcriptome assembly of a single V. vinifera cultivar is insufficient for a complete genome annotation of the grapevine reference genome constructed from V. vinifera PN40024. Further, we provide evidence that the gene models we identified cannot be completely anchored to the previously published V. vinifera PN40024 gene models. In addition to these findings, we present a computational pipeline for the de novo identification of lncRNAs. Our results demonstrate that, in grapevine, lncRNAs are significantly different from protein coding transcripts in such metrics as length, GC-content, minimum free energy, and length-corrected minimum free energy.

Conclusions: In grapevine, high-level heterozygosity necessitates that transcriptome characterization be based on cultivar-specific reference genome sequences. Our results strengthen the hypothesis that lncRNAs have thermodynamically different properties than protein-coding RNAs. The analyses of both coding and non-coding RNAs will be instrumental in uncovering inter-cultivar variation in wild and cultivated grapevine species.
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http://dx.doi.org/10.1186/s12864-017-4346-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5712117PMC
December 2017

A next-generation marker genotyping platform (AmpSeq) in heterozygous crops: a case study for marker-assisted selection in grapevine.

Hortic Res 2016 17;3:16002. Epub 2016 Feb 17.

Bioinformatics Facility, Cornell University , Ithaca, NY 14853, USA.

Marker-assisted selection (MAS) is often employed in crop breeding programs to accelerate and enhance cultivar development, via selection during the juvenile phase and parental selection prior to crossing. Next-generation sequencing and its derivative technologies have been used for genome-wide molecular marker discovery. To bridge the gap between marker development and MAS implementation, this study developed a novel practical strategy with a semi-automated pipeline that incorporates trait-associated single nucleotide polymorphism marker discovery, low-cost genotyping through amplicon sequencing (AmpSeq) and decision making. The results document the development of a MAS package derived from genotyping-by-sequencing using three traits (flower sex, disease resistance and acylated anthocyanins) in grapevine breeding. The vast majority of sequence reads (⩾99%) were from the targeted regions. Across 380 individuals and up to 31 amplicons sequenced in each lane of MiSeq data, most amplicons (83 to 87%) had <10% missing data, and read depth had a median of 220-244×. Several strengths of the AmpSeq platform that make this approach of broad interest in diverse crop species include accuracy, flexibility, speed, high-throughput, low-cost and easily automated analysis.
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http://dx.doi.org/10.1038/hortres.2016.2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4879517PMC
June 2016

Next Generation Mapping of Enological Traits in an F2 Interspecific Grapevine Hybrid Family.

PLoS One 2016 14;11(3):e0149560. Epub 2016 Mar 14.

Plant Science Department, South Dakota State University, Brookings, South Dakota, United States of America.

In winegrapes (Vitis spp.), fruit quality traits such as berry color, total soluble solids content (SS), malic acid content (MA), and yeast assimilable nitrogen (YAN) affect fermentation or wine quality, and are important traits in selecting new hybrid winegrape cultivars. Given the high genetic diversity and heterozygosity of Vitis species and their tendency to exhibit inbreeding depression, linkage map construction and quantitative trait locus (QTL) mapping has relied on F1 families with the use of simple sequence repeat (SSR) and other markers. This study presents the construction of a genetic map by single nucleotide polymorphisms identified through genotyping-by-sequencing (GBS) technology in an F2 mapping family of 424 progeny derived from a cross between the wild species V. riparia Michx. and the interspecific hybrid winegrape cultivar, 'Seyval'. The resulting map has 1449 markers spanning 2424 cM in genetic length across 19 linkage groups, covering 95% of the genome with an average distance between markers of 1.67 cM. Compared to an SSR map previously developed for this F2 family, these results represent an improved map covering a greater portion of the genome with higher marker density. The accuracy of the map was validated using the well-studied trait berry color. QTL affecting YAN, MA and SS related traits were detected. A joint MA and SS QTL spans a region with candidate genes involved in the malate metabolism pathway. We present an analytical pipeline for calling intercross GBS markers and a high-density linkage map for a large F2 family of the highly heterozygous Vitis genus. This study serves as a model for further genetic investigations of the molecular basis of additional unique characters of North American hybrid wine cultivars and to enhance the breeding process by marker-assisted selection. The GBS protocols for identifying intercross markers developed in this study can be adapted for other heterozygous species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0149560PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4790954PMC
August 2016

Climate and Developmental Plasticity: Interannual Variability in Grapevine Leaf Morphology.

Plant Physiol 2016 Mar 29;170(3):1480-91. Epub 2016 Jan 29.

Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (D.H.C., S.M.R., D.Y.L., Q.L.W., T.T.Y., D.G.); University of Northern Iowa, Department of Biology, Cedar Falls, Iowa 50614 (J.R.L., J.K.); andU.S. Department of Agriculture, Agriculture Research Service, Grape Genetics Research Unit, Geneva, New York 14456 (J.P.L.).

The shapes of leaves are dynamic, changing over evolutionary time between species, within a single plant producing different shaped leaves at successive nodes, during the development of a single leaf as it allometrically expands, and in response to the environment. Notably, strong correlations between the dissection and size of leaves with temperature and precipitation exist in both the paleorecord and extant populations. Yet, a morphometric model integrating evolutionary, developmental, and environmental effects on leaf shape is lacking. Here, we continue a morphometric analysis of >5,500 leaves representing 270 grapevines of multiple Vitis species between two growing seasons. Leaves are paired one-to-one and vine-to-vine accounting for developmental context, between growing seasons. Linear discriminant analysis reveals shape features that specifically define growing season, regardless of species or developmental context. The shape feature, a more pronounced distal sinus, is associated with the colder, drier growing season, consistent with patterns observed in the paleorecord. We discuss the implications of such plasticity in a long-lived woody perennial, such as grapevine (Vitis spp.), with respect to the evolution and functionality of plant morphology and changes in climate.
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http://dx.doi.org/10.1104/pp.15.01825DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4775139PMC
March 2016

Rootstocks: Diversity, Domestication, and Impacts on Shoot Phenotypes.

Trends Plant Sci 2016 05 11;21(5):418-437. Epub 2015 Dec 11.

Saint Louis University, Department of Biology, 3507 Laclede Avenue, St. Louis, MO 63103-2010, USA; Missouri Botanical Garden, 4344 Shaw Boulevard, St. Louis, MO 63110-2226, USA. Electronic address:

Grafting is an ancient agricultural practice that joins the root system (rootstock) of one plant to the shoot (scion) of another. It is most commonly employed in woody perennial crops to indirectly manipulate scion phenotype. While recent research has focused on scions, here we investigate rootstocks, the lesser-known half of the perennial crop equation. We review natural grafting, grafting in agriculture, rootstock diversity and domestication, and developing areas of rootstock research, including molecular interactions and rootstock microbiomes. With growing interest in perennial crops as valuable components of sustainable agriculture, rootstocks provide one mechanism by which to improve and expand woody perennial cultivation in a range of environmental conditions.
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http://dx.doi.org/10.1016/j.tplants.2015.11.008DOI Listing
May 2016

Latent developmental and evolutionary shapes embedded within the grapevine leaf.

New Phytol 2016 Apr 18;210(1):343-55. Epub 2015 Nov 18.

United States Department of Agriculture, Agriculture Research Service, Grape Genetics Research Unit, Geneva, NY, 14456, USA.

Across plants, leaves exhibit profound diversity in shape. As a single leaf expands, its shape is in constant flux. Plants may also produce leaves with different shapes at successive nodes. In addition, leaf shape varies among individuals, populations and species as a result of evolutionary processes and environmental influences. Because leaf shape can vary in many different ways, theoretically, the effects of distinct developmental and evolutionary processes are separable, even within the shape of a single leaf. Here, we measured the shapes of > 3200 leaves representing > 270 vines from wild relatives of domesticated grape (Vitis spp.) to determine whether leaf shapes attributable to genetics and development are separable from each other. We isolated latent shapes (multivariate signatures that vary independently from each other) embedded within the overall shape of leaves. These latent shapes can predict developmental stages independent from species identity and vice versa. Shapes predictive of development were then used to stage leaves from 1200 varieties of domesticated grape (Vitis vinifera), revealing that changes in timing underlie leaf shape diversity. Our results indicate that distinct latent shapes combine to produce a composite morphology in leaves, and that developmental and evolutionary contributions to shape vary independently from each other.
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http://dx.doi.org/10.1111/nph.13754DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5063178PMC
April 2016

Heterozygous Mapping Strategy (HetMappS) for High Resolution Genotyping-By-Sequencing Markers: A Case Study in Grapevine.

PLoS One 2015 5;10(8):e0134880. Epub 2015 Aug 5.

USDA-ARS Grape Genetics Research Unit, Geneva, New York, United States of America.

Genotyping by sequencing (GBS) provides opportunities to generate high-resolution genetic maps at a low genotyping cost, but for highly heterozygous species, missing data and heterozygote undercalling complicate the creation of GBS genetic maps. To overcome these issues, we developed a publicly available, modular approach called HetMappS, which functions independently of parental genotypes and corrects for genotyping errors associated with heterozygosity. For linkage group formation, HetMappS includes both a reference-guided synteny pipeline and a reference-independent de novo pipeline. The de novo pipeline can be utilized for under-characterized or high diversity families that lack an appropriate reference. We applied both HetMappS pipelines in five half-sib F1 families involving genetically diverse Vitis spp. Starting with at least 116,466 putative SNPs per family, the HetMappS pipelines identified 10,440 to 17,267 phased pseudo-testcross (Pt) markers and generated high-confidence maps. Pt marker density exceeded crossover resolution in all cases; up to 5,560 non-redundant markers were used to generate parental maps ranging from 1,047 cM to 1,696 cM. The number of markers used was strongly correlated with family size in both de novo and synteny maps (r = 0.92 and 0.91, respectively). Comparisons between allele and tag frequencies suggested that many markers were in tandem repeats and mapped as single loci, while markers in regions of more than two repeats were removed during map curation. Both pipelines generated similar genetic maps, and genetic order was strongly correlated with the reference genome physical order in all cases. Independently created genetic maps from shared parents exhibited nearly identical results. Flower sex was mapped in three families and correctly localized to the known sex locus in all cases. The HetMappS pipeline could have wide application for genetic mapping in highly heterozygous species, and its modularity provides opportunities to adapt portions of the pipeline to other family types, genotyping technologies or applications.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0134880PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4526651PMC
May 2016

Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera.

BMC Plant Biol 2014 Apr 22;14:103. Epub 2014 Apr 22.

Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan, PR China.

Background: WRKY transcription factors are one of the largest families of transcriptional regulators in plants. WRKY genes are not only found to play significant roles in biotic and abiotic stress response, but also regulate growth and development. Grapevine (Vitis vinifera) production is largely limited by stressful climate conditions such as cold stress and the role of WRKY genes in the survival of grapevine under these conditions remains unknown.

Results: We identified a total of 59 VvWRKYs from the V. vinifera genome, belonging to four subgroups according to conserved WRKY domains and zinc-finger structure. The majority of VvWRKYs were expressed in more than one tissue among the 7 tissues examined which included young leaves, mature leaves, tendril, stem apex, root, young fruits and ripe fruits. Publicly available microarray data suggested that a subset of VvWRKYs was activated in response to diverse stresses. Quantitative real-time PCR (qRT-PCR) results demonstrated that the expression levels of 36 VvWRKYs are changed following cold exposure. Comparative analysis was performed on data from publicly available microarray experiments, previous global transcriptome analysis studies, and qRT-PCR. We identified 15 VvWRKYs in at least two of these databases which may relate to cold stress. Among them, the transcription of three genes can be induced by exogenous ABA application, suggesting that they can be involved in an ABA-dependent signaling pathway in response to cold stress.

Conclusions: We identified 59 VvWRKYs from the V. vinifera genome and 15 of them showed cold stress-induced expression patterns. These genes represented candidate genes for future functional analysis of VvWRKYs involved in the low temperature-related signal pathways in grape.
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http://dx.doi.org/10.1186/1471-2229-14-103DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4021059PMC
April 2014

Sub-lethal glyphosate exposure alters flowering phenology and causes transient male-sterility in Brassica spp.

BMC Plant Biol 2014 Mar 21;14:70. Epub 2014 Mar 21.

USDA-ARS Grape Genetics Research Unit, Geneva, NY 14456, USA.

Background: Herbicide resistance in weedy plant populations can develop through different mechanisms such as gene flow of herbicide resistance transgenes from crop species into compatible weedy species or by natural evolution of herbicide resistance or tolerance following selection pressure. Results from our previous studies suggest that sub-lethal levels of the herbicide glyphosate can alter the pattern of gene flow between glyphosate resistant Canola®, Brassica napus, and glyphosate sensitive varieties of B. napus and B. rapa. The objectives of this study were to examine the phenological and developmental changes that occur in Brassica crop and weed species following sub-lethal doses of the herbicides glyphosate and glufosinate. We examined several vegetative and reproductive traits of potted plants under greenhouse conditions, treated with sub-lethal herbicide sprays.

Results: Our results indicate that exposure of Brassica spp. to a sub-lethal dose of glyphosate results in altering flowering phenology and reproductive function. Flowering of all sensitive species was significantly delayed and reproductive function, specifically male fertility, was suppressed. Higher dosage levels typically contributed to an increase in the magnitude of phenotypic changes.

Conclusions: These results demonstrate that Brassica spp. plants that are exposed to sub-lethal doses of glyphosate could be subject to very different pollination patterns and an altered pattern of gene flow that would result from changes in the overlap of flowering phenology between species. Implications include the potential for increased glyphosate resistance evolution and spread in weedy communities exposed to sub-lethal glyphosate.
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http://dx.doi.org/10.1186/1471-2229-14-70DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3998022PMC
March 2014

Genome wide transcriptional profile analysis of Vitis amurensis and Vitis vinifera in response to cold stress.

PLoS One 2013 13;8(3):e58740. Epub 2013 Mar 13.

Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, The Chinese Academy of Sciences, Wuhan, P. R. China.

Grape is one of the most important fruit crops worldwide. The suitable geographical locations and productivity of grapes are largely limited by temperature. Vitis amurensis is a wild grapevine species with remarkable cold-tolerance, exceeding that of Vitis vinifera, the dominant cultivated species of grapevine. However, the molecular mechanisms that contribute to the enhanced freezing tolerance of V. amurensis remain unknown. Here we used deep sequencing data from restriction endonuclease-generated cDNA fragments to evaluate the whole genome wide modification of transcriptome of V. amurensis under cold treatment. Vitis vinifera cv. Muscat of Hamburg was used as control to help investigate the distinctive features of V. amruensis in responding to cold stress. Approximately 9 million tags were sequenced from non-cold treatment (NCT) and cold treatment (CT) cDNA libraries in each species of grapevine sampled from shoot apices. Alignment of tags into V. vinifera cv. Pinot noir (PN40024) annotated genome identified over 15,000 transcripts in each library in V. amruensis and more than 16,000 in Muscat of Hamburg. Comparative analysis between NCT and CT libraries indicate that V. amurensis has fewer differential expressed genes (DEGs, 1314 transcripts) than Muscat of Hamburg (2307 transcripts) when exposed to cold stress. Common DEGs (408 transcripts) suggest that some genes provide fundamental roles during cold stress in grapes. The most robust DEGs (more than 20-fold change) also demonstrated significant differences between two kinds of grapevine, indicating that cold stress may trigger species specific pathways in V. amurensis. Functional categories of DEGs indicated that the proportion of up-regulated transcripts related to metabolism, transport, signal transduction and transcription were more abundant in V. amurensis. Several highly expressed transcripts that were found uniquely accumulated in V. amurensis are discussed in detail. This subset of unique candidate transcripts may contribute to the excellent cold-hardiness of V. amurensis.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0058740PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3596283PMC
September 2013

The establishment of genetically engineered canola populations in the U.S.

PLoS One 2011 5;6(10):e25736. Epub 2011 Oct 5.

Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas, United States of America.

Concerns regarding the commercial release of genetically engineered (GE) crops include naturalization, introgression to sexually compatible relatives and the transfer of beneficial traits to native and weedy species through hybridization. To date there have been few documented reports of escape leading some researchers to question the environmental risks of biotech products. In this study we conducted a systematic roadside survey of canola (Brassica napus) populations growing outside of cultivation in North Dakota, USA, the dominant canola growing region in the U.S. We document the presence of two escaped, transgenic genotypes, as well as non-GE canola, and provide evidence of novel combinations of transgenic forms in the wild. Our results demonstrate that feral populations are large and widespread. Moreover, flowering times of escaped populations, as well as the fertile condition of the majority of collections suggest that these populations are established and persistent outside of cultivation.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0025736PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3187797PMC
February 2012

Changes in constructed Brassica communities treated with glyphosate drift.

Ecol Appl 2011 Mar;21(2):525-38

U.S. Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Western Ecology Division, 200 SW 35th Street, Corvallis, Oregon 97333, USA.

We constructed a mixed-species community designed to simulate roadside and field edge plant communities and exposed it to glyphosate drift in order to test three hypotheses: (1) higher fitness in transgenic Brassica carrying the CP4 EPSPS transgene that confers resistance to glyphosate will result in significant changes in the plant community relative to control communities; (2) given repeated years of glyphosate drift selective pressure, the increased fitness of the transgenic Brassica with CP4 EPSPS will contribute to an increase in the proportion of transgenic progeny produced in plant communities; and (3) the increased fitness of Brassica carrying the CP4 EPSPS transgene will contribute to decreased levels of mycorrhizal infection and biomass in a host species (Trifolium incarnatum). Due to regulatory constraints that prevented the use of outdoor plots for our studies, in 2005 we established multispecies communities in five large cylindrical outdoor sunlit mesocosms (plastic greenhouses) designed for pollen confinement. Three of the community members were sexually compatible Brassica spp.: transgenic glyphosate-resistant canola (B. napus) cultivar (cv.) RaideRR, glyphosate-sensitive non-transgenic B. napus cv. Sponsor, and a weedy B. rapa (GRIN Accession 21735). Additional plant community members were the broadly distributed annual weeds Digitaria sanguinalis, Panicum capillare, and Lapsana communis. Once annually in 2006 and 2007, two mesocosms were sprayed with glyphosate at 10% of the field application rate to simulate glyphosate drift as a selective pressure. After two years, changes were observed in community composition, plant density, and biomass in both control and treatment mesocosms. In control mesocosms, the weed D. sanguinalis (crabgrass) began to dominate. In glyphosate drift-treated mesocosms, Brassica remained the dominant genus and the incidence of the CP4 EPSPS transgene increased in the community. Shoot biomass and mycorrhizal infection in Trifolium incarnatum planted in 2008 were significantly lower in mesocosms that had received glyphosate drift treatments. Our results suggest that, over time, glyphosate drift can contribute to persistence of Brassica that express the CP4 EPSPS transgene and that increased representation of Brassica (a non-mycorrhizal host) within plant communities may indirectly negatively impact beneficial ecosystem services associated with arbuscular mycorrhiza.
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http://dx.doi.org/10.1890/09-2366.1DOI Listing
March 2011

Glyphosate-drift but not herbivory alters the rate of transgene flow from single and stacked trait transgenic canola (Brassica napus) to nontransgenic B. napus and B. rapa.

New Phytol 2011 Aug 28;191(3):840-849. Epub 2011 Mar 28.

US Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Western Ecology Division, 200 SW 35th Street Corvallis, OR 97333, USA.

• Transgenic plants can offer agricultural benefits, but the escape of transgenes is an environmental concern. In this study we tested the hypothesis that glyphosate drift and herbivory selective pressures can change the rate of transgene flow between the crop Brassica napus (canola), and weedy species and contribute to the potential for increased transgene escape risk and persistence outside of cultivation. • We constructed plant communities containing single transgenic B. napus genotypes expressing glyphosate herbicide resistance (CP4 EPSPS), lepidopteran insect resistance (Cry1Ac), or both traits ('stacked'), plus nontransgenic B. napus, Brassica rapa and Brassica nigra. Two different selective pressures, a sublethal glyphosate dose and lepidopteran herbivores (Plutella xylostella), were applied and rates of transgene flow and transgenic seed production were measured. • Selective treatments differed in the degree in which they affected gene flow and production of transgenic hybrid seed. Most notably, glyphosate-drift increased the incidence of transgenic seeds on nontransgenic B. napus by altering flowering phenology and reproductive function. • The findings of this study indicate that transgenic traits may be transmitted to wild populations and may increase in frequency in weedy populations through the direct and indirect effects of selection pressures on gene flow.
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http://dx.doi.org/10.1111/j.1469-8137.2011.03706.xDOI Listing
August 2011
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