Publications by authors named "Daniel H Chitwood"

64 Publications

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

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

The influences of environmental change and development on leaf shape in Vitis.

Am J Bot 2020 04 9;107(4):676-688. Epub 2020 Apr 9.

Terrestrial Paleoclimate Research Group, Department of Geosciences, Baylor University, Waco, TX, USA.

Premise: The size and shape (physiognomy) of woody, dicotyledonous angiosperm leaves are correlated with climate. These relationships are the basis for multiple paleoclimate proxies. Here we test whether Vitis exhibits phenotypic plasticity and whether physiognomy varies along the vine.

Methods: We used Digital Leaf Physiognomy (DiLP) to measure leaf characters of four Vitis species from the USDA Germplasm Repository (Geneva, New York) from the 2012-2013 and 2014-2015 leaf-growing seasons, which had different environmental conditions.

Results: Leaf shape changed allometrically through developmental stages; early stages were more linear than later stages. There were significant differences in physiognomy in the same developmental stage between the growing seasons, and species had significant differences in mean physiognomy between growing seasons. Phenotypic plasticity was defined as changes between growing seasons after controlling for developmental stage or after averaging all developmental stages. Vitis amurensis and V. riparia had the greatest phenotypic plasticity. North American species exhibited significant differences in tooth area:blade area. Intermediate developmental stages were most likely to exhibit phenotypic plasticity, and only V. amurensis exhibited phenotypic plasticity in later developmental stages.

Conclusions: Leaves have variable phenotypic plasticity along the vine. Environmental signal was strongest in intermediate developmental stages. This is significant for leaf physiognomic-paleoclimate proxies because these leaves are likely the most common in leaf litter and reflect leaves primarily included in paleoclimate reconstructions. Early season and early developmental stages have the potential to be confounding factors but are unlikely to exert significant influence because of differential preservation potential.
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http://dx.doi.org/10.1002/ajb2.1460DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7217169PMC
April 2020

The shape of things to come: Topological data analysis and biology, from molecules to organisms.

Dev Dyn 2020 07 13;249(7):816-833. Epub 2020 Apr 13.

Department of Computational Mathematics, Science & Engineering, Michigan State University, East Lansing, Michigan, USA.

Shape is data and data is shape. Biologists are accustomed to thinking about how the shape of biomolecules, cells, tissues, and organisms arise from the effects of genetics, development, and the environment. Less often do we consider that data itself has shape and structure, or that it is possible to measure the shape of data and analyze it. Here, we review applications of topological data analysis (TDA) to biology in a way accessible to biologists and applied mathematicians alike. TDA uses principles from algebraic topology to comprehensively measure shape in data sets. Using a function that relates the similarity of data points to each other, we can monitor the evolution of topological features-connected components, loops, and voids. This evolution, a topological signature, concisely summarizes large, complex data sets. We first provide a TDA primer for biologists before exploring the use of TDA across biological sub-disciplines, spanning structural biology, molecular biology, evolution, and development. We end by comparing and contrasting different TDA approaches and the potential for their use in biology. The vision of TDA, that data are shape and shape is data, will be relevant as biology transitions into a data-driven era where the meaningful interpretation of large data sets is a limiting factor.
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http://dx.doi.org/10.1002/dvdy.175DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7383827PMC
July 2020

Leaf shape is a predictor of fruit quality and cultivar performance in tomato.

New Phytol 2020 05 11;226(3):851-865. Epub 2020 Feb 11.

Department of Plant Biology, University of California, Davis, CA, 95616, USA.

Commercial tomato (Solanum lycopersicum) is one of the most widely grown vegetable crops worldwide. Heirloom tomatoes retain extensive genetic diversity and a considerable range of fruit quality and leaf morphological traits. Here the role of leaf morphology was investigated for its impact on fruit quality. Heirloom cultivars were grown in field conditions, and BRIX by yield (BY) and other traits were measured over a 14-wk period. The complex relationships among these morphological and physiological traits were evaluated using partial least-squares path modeling, and a consensus model was developed. Photosynthesis contributed strongly to vegetative biomass and sugar content of fruits but had a negative impact on yield. Conversely leaf shape, specifically rounder leaves, had a strong positive impact on both fruit sugar content and yield. Cultivars such as Stupice and Glacier, with very round leaves, had the highest performance in both fruit sugar and yield. Our model accurately predicted BY for two commercial cultivars using leaf shape data as input. This study revealed the importance of leaf shape to fruit quality in tomato, with rounder leaves having significantly improved fruit quality. This correlation was maintained across a range of diverse genetic backgrounds and shows the importance of leaf morphology in tomato crop improvement.
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http://dx.doi.org/10.1111/nph.16403DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7187315PMC
May 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

Isolating phyllotactic patterns embedded in the secondary growth of sweet cherry ( L.) using magnetic resonance imaging.

Plant Methods 2019 4;15:111. Epub 2019 Oct 4.

1Department of Computational Mathematics, Science and Engineering, Michigan State University, East Lansing, MI 48824 USA.

Background: Epicormic branches arise from dormant buds patterned during the growth of previous years. Dormant epicormic buds remain just below the surface of trees, pushed outward from the pith during secondary growth, but maintain vascular connections. Epicormic buds can be activated to elongate into a new shoot, either through natural processes or horticultural intervention, to potentially rejuvenate orchards and restructure tree architecture. Because epicormic structures are embedded within secondary growth, tomographic approaches are a useful method to study them and understand their development.

Results: We apply techniques from image processing to determine the locations of epicormic vascular traces embedded within secondary growth of sweet cherry ( L.), revealing the juvenile phyllotactic pattern in the trunk of an adult tree. Techniques include the flood fill algorithm to find the pith of the tree, edge detection to approximate the radius, and a conversion to polar coordinates to threshold and segment phyllotactic features. Intensity values from magnetic resonance imaging (MRI) of the trunk are projected onto the surface of a perfect cylinder to find the locations of traces in the "boundary image". Mathematical phyllotaxy provides a means to capture the patterns in the boundary image by modeling phyllotactic parameters. Our cherry tree specimen has the conspicuous parastichy pair (2,3), phyllotactic fraction 2/5, and divergence angle of approximately 143°.

Conclusions: The methods described provide a framework not only for studying phyllotaxy, but also for processing of volumetric image data in plants. Our results have practical implications for orchard rejuvenation and directed approaches to influence tree architecture. The study of epicormic structures, which are hidden within secondary growth, using tomographic methods also opens the possibility of studying genetic and environmental influences such structures.
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http://dx.doi.org/10.1186/s13007-019-0496-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6777031PMC
October 2019

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

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

Long-Distance and Trans-Generational Stomatal Patterning by CO Across Organs.

Front Plant Sci 2018 30;9:1714. Epub 2018 Nov 30.

Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, United States.

Stomata control water loss and carbon dioxide uptake by both altering pore aperture and developmental patterning. Stomatal patterning is regulated by environmental factors including atmospheric carbon dioxide ([CO]), which is increasing globally at an unprecedented rate. Mature leaves are known to convey developmental cues to immature leaves in response to [CO], but the developmental mechanisms are unknown. To characterize changes in stomatal patterning resulting from signals moving from mature to developing leaves, we constructed a dual-chamber growth system in which rosette and cauline leaves of were subjected to differing [CO]. Young rosette tissue was found to adjust stomatal index (SI, the proportion of stomata to total cell number) in response to both the current environment and the environment experienced by mature rosette tissue, whereas cauline leaves appear to be insensitive to [CO] treatment. It is likely that cauline leaves and cotyledons deploy mechanisms for controlling stomatal development that share common but also deploy distinctive mechanisms to that operating in rosette leaves. The effect of [CO] on stomatal development is retained in cotyledons of the next generation, however, this effect does not occur in pre-germination stomatal lineage cells but only after germination. Finally, these data suggest that [CO] affects regulation of stomatal development specifically through the development of satellite stomata (stomata induced by signals from a neighboring stomate) during spacing divisions and not the basal pathway. To our knowledge, this is the first report identifying developmental steps responsible for altered stomatal patterning to [CO] and its trans-generational inheritance.
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http://dx.doi.org/10.3389/fpls.2018.01714DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6287203PMC
November 2018

Bundle sheath extensions affect leaf structural and physiological plasticity in response to irradiance.

Plant Cell Environ 2019 05 19;42(5):1575-1589. Epub 2019 Feb 19.

Departamento de Biologia Vegetal, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, MG, Brazil.

Coordination between structural and physiological traits is key to plants' responses to environmental fluctuations. In heterobaric leaves, bundle sheath extensions (BSEs) increase photosynthetic performance (light-saturated rates of photosynthesis, A ) and water transport capacity (leaf hydraulic conductance, K ). However, it is not clear how BSEs affect these and other leaf developmental and physiological parameters in response to environmental conditions. The obscuravenosa (obv) mutation, found in many commercial tomato varieties, leads to absence of BSEs. We examined structural and physiological traits of tomato heterobaric and homobaric (obv) near-isogenic lines grown at two different irradiance levels. K , minor vein density, and stomatal pore area index decreased with shading in heterobaric but not in homobaric leaves, which show similarly lower values in both conditions. Homobaric plants, on the other hand, showed increased A , leaf intercellular air spaces, and mesophyll surface area exposed to intercellular airspace (S ) in comparison with heterobaric plants when both were grown in the shade. BSEs further affected carbon isotope discrimination, a proxy for long-term water-use efficiency. BSEs confer plasticity in traits related to leaf structure and function in response to irradiance levels and might act as a hub integrating leaf structure, photosynthetic function, and water supply and demand.
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http://dx.doi.org/10.1111/pce.13495DOI Listing
May 2019

Gating of miRNA movement at defined cell-cell interfaces governs their impact as positional signals.

Nat Commun 2018 08 6;9(1):3107. Epub 2018 Aug 6.

Cold Spring Harbor Laboratory, One Bungtown Road, Cold Spring Harbor, NY, 11724, USA.

Mobile small RNAs serve as local positional signals in development and coordinate stress responses across the plant. Despite its central importance, an understanding of how the cell-to-cell movement of small RNAs is governed is lacking. Here, we show that miRNA mobility is precisely regulated through a gating mechanism polarised at defined cell-cell interfaces. This generates directional movement between neighbouring cells that limits long-distance shoot-to-root trafficking, and underpins domain-autonomous behaviours of small RNAs within stem cell niches. We further show that the gating of miRNA mobility occurs independent of mechanisms controlling protein movement, identifying the small RNA as the mobile unit. These findings reveal gate-keepers of cell-to-cell small RNA mobility generate selectivity in long-distance signalling, and help safeguard functional domains within dynamic stem cell niches while mitigating a 'signalling gridlock' in contexts where developmental patterning events occur in close spatial and temporal vicinity.
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http://dx.doi.org/10.1038/s41467-018-05571-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6079027PMC
August 2018

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

The Persistent Homology Mathematical Framework Provides Enhanced Genotype-to-Phenotype Associations for Plant Morphology.

Plant Physiol 2018 08 5;177(4):1382-1395. Epub 2018 Jun 5.

Donald Danforth Plant Science Center, St. Louis, Missouri 63132

Efforts to understand the genetic and environmental conditioning of plant morphology are hindered by the lack of flexible and effective tools for quantifying morphology. Here, we demonstrate that persistent-homology-based topological methods can improve measurement of variation in leaf shape, serrations, and root architecture. We apply these methods to 2D images of leaves and root systems in field-grown plants of a domesticated introgression line population of tomato (). We find that compared with some commonly used conventional traits, (1) persistent-homology-based methods can more comprehensively capture morphological variation; (2) these techniques discriminate between genotypes with a larger normalized effect size and detect a greater number of unique quantitative trait loci (QTLs); (3) multivariate traits, whether statistically derived from univariate or persistent-homology-based traits, improve our ability to understand the genetic basis of phenotype; and (4) persistent-homology-based techniques detect unique QTLs compared to conventional traits or their multivariate derivatives, indicating that previously unmeasured aspects of morphology are now detectable. The QTL results further imply that genetic contributions to morphology can affect both the shoot and root, revealing a pleiotropic basis to natural variation in tomato. Persistent homology is a versatile framework to quantify plant morphology and developmental processes that complements and extends existing methods.
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http://dx.doi.org/10.1104/pp.18.00104DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6084663PMC
August 2018

Genetic and Developmental Basis for Increased Leaf Thickness in the Arabidopsis Cvi Ecotype.

Front Plant Sci 2018 14;9:322. Epub 2018 Mar 14.

Donald Danforth Plant Science Center, St. Louis, MO, United States.

Leaf thickness is a quantitative trait that is associated with the ability of plants to occupy dry, high irradiance environments. Despite its importance, leaf thickness has been difficult to measure reproducibly, which has impeded progress in understanding its genetic basis, and the associated anatomical mechanisms that pattern it. Here, we used a custom-built dual confocal profilometer device to measure leaf thickness in the Arabidopsis Ler × Cvi recombinant inbred line population and found statistical support for four quantitative trait loci (QTL) associated with this trait. We used publically available data for a suite of traits relating to flowering time and growth responses to light quality and show that three of the four leaf thickness QTL coincide with QTL for at least one of these traits. Using time course photography, we quantified the relative growth rate and the pace of rosette leaf initiation in the Ler and Cvi ecotypes. We found that Cvi rosettes grow slower than Ler, both in terms of the rate of leaf initiation and the overall rate of biomass accumulation. Collectively, these data suggest that leaf thickness is tightly linked with physiological status and may present a tradeoff between the ability to withstand stress and rapid vegetative growth. To understand the anatomical basis of leaf thickness, we compared cross-sections of Cvi and Ler leaves and show that Cvi palisade mesophyll cells elongate anisotropically contributing to leaf thickness. Flow cytometry of whole leaves show that endopolyploidy accompanies thicker leaves in Cvi. Overall, our data suggest that mechanistically, an altered schedule of cellular events affecting endopolyploidy and increasing palisade mesophyll cell length contribute to increase of leaf thickness in Cvi. Ultimately, knowledge of the genetic basis and developmental trajectory leaf thickness will inform the mechanisms by which natural selection acts to produce variation in this adaptive trait.
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http://dx.doi.org/10.3389/fpls.2018.00322DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5861201PMC
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

Divergent leaf shapes among species arise from a shared juvenile morphology.

Plant Direct 2017 Nov 6;1(5):e00028. Epub 2017 Nov 6.

Departamento de Biologia Vegetal/BIOAGRO Universidade Federal de Viçosa Viçosa MG Brasil.

Not only does leaf shape vary between species, but between sequential nodes of the vine. The profound changes in leaf shape within vines reflect the temporal development of the shoot apical meristem from which leaves are derived and patterned, a phenomenon known as heteroblasty. We perform a morphometric analysis of more than 3,300 leaves from 40 different species using two different methods: homologous landmarks and Elliptical Fourier Descriptors (EFDs). Changes in leaf shape across the vine are first quantified in allometric terms; that is, changes in the relative area of leaf subregions expressed in terms of overall leaf area. Shape is constrained to strict linear relationships as a function of size that vary between species. Statistical analysis of leaf shape, using landmarks and EFDs, reveals that species effects (regardless of node) are the strongest, followed by interaction effects between species and heteroblasty (i.e., species-specific patterns in leaf shape across nodes) and that heteroblasty effects across nodes (regardless of species) are negligible. The ability of different nodes to predictively discriminate species and the variability of landmark and EFD traits at each node is then analyzed. Heteroblastic trajectories, the changes in leaf shape between the first and last measured leaves in a vine, are then compared between species in a multivariate space. Leaf shape diversity among species is expressed in a heteroblastic-dependent manner, unique to each species. Leaf shape is constrained by linear, allometric relationships related to leaf size that vary between species. There is a strong species × heteroblasty interaction effect for leaf shape, suggesting that different leaf shapes between species arise through changes in shape across nodes specific to each species. The first leaves in the series are not only more like each other, but are also less variable across species. From this similar, shared leaf shape, subsequent leaves in the heteroblastic series follow divergent morphological trajectories. The disparate leaf shapes characteristic of species arise from a shared, juvenile morphology.
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http://dx.doi.org/10.1002/pld3.28DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6508542PMC
November 2017

Erratum to: Morphometric analysis of Passiflora leaves: the relationship between landmarks of the vasculature and elliptical Fourier descriptors of the blade.

Gigascience 2017 10;6(10)

Background: Leaf shape among Passiflora species is spectacularly diverse. Underlying this diversity in leaf shape are profound changes in the patterning of the primary vasculature and laminar outgrowth. Each of these aspects of leaf morphology-vasculature and blade-provides different insights into leaf patterning.

Results: Here, we morphometrically analyze >3300 leaves from 40 different Passiflora species collected sequentially across the vine. Each leaf is measured in two different ways: using 1) 15 homologous Procrustes-adjusted landmarks of the vasculature, sinuses, and lobes; and 2) Elliptical Fourier Descriptors (EFDs), which quantify the outline of the leaf. The ability of landmarks, EFDs, and both datasets together are compared to determine their relative ability to predict species and node position within the vine. Pairwise correlation of x and y landmark coordinates and EFD harmonic coefficients reveals close associations between traits and insights into the relationship between vasculature and blade patterning.

Conclusions: Landmarks, more reflective of the vasculature, and EFDs, more reflective of the blade contour, describe both similar and distinct features of leaf morphology. Landmarks and EFDs vary in ability to predict species identity and node position in the vine and exhibit a correlational structure (both within landmark or EFD traits and between the two data types) revealing constraints between vascular and blade patterning underlying natural variation in leaf morphology among Passiflora species.
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http://dx.doi.org/10.1093/gigascience/gix070DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5632300PMC
October 2017

Genetic Architecture and Molecular Networks Underlying Leaf Thickness in Desert-Adapted Tomato .

Plant Physiol 2017 Sep 9;175(1):376-391. Epub 2017 Aug 9.

Donald Danforth Plant Science Center, St. Louis, Missouri 63132

Thicker leaves allow plants to grow in water-limited conditions. However, our understanding of the genetic underpinnings of this highly functional leaf shape trait is poor. We used a custom-built confocal profilometer to directly measure leaf thickness in a set of introgression lines (ILs) derived from the desert tomato and identified quantitative trait loci. We report evidence of a complex genetic architecture of this trait and roles for both genetic and environmental factors. Several ILs with thick leaves have dramatically elongated palisade mesophyll cells and, in some cases, increased leaf ploidy. We characterized the thick IL2-5 and IL4-3 in detail and found increased mesophyll cell size and leaf ploidy levels, suggesting that endoreduplication underpins leaf thickness in tomato. Next, we queried the transcriptomes and inferred dynamic Bayesian networks of gene expression across early leaf ontogeny in these lines to compare the molecular networks that pattern leaf thickness. We show that thick ILs share -like expression profiles for putative regulators of cell shape and meristem determinacy as well as a general signature of cell cycle-related gene expression. However, our network data suggest that leaf thickness in these two lines is patterned at least partially by distinct mechanisms. Consistent with this hypothesis, double homozygote lines combining introgression segments from these two ILs show additive phenotypes, including thick leaves, higher ploidy levels, and larger palisade mesophyll cells. Collectively, these data establish a framework of genetic, anatomical, and molecular mechanisms that pattern leaf thickness in desert-adapted tomato.
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http://dx.doi.org/10.1104/pp.17.00790DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5580771PMC
September 2017

Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences.

Front Plant Sci 2017 9;8:900. Epub 2017 Jun 9.

Department of Remote Sensing and Photogrammetry, Finnish Geospatial Research Institute, National Land Survey of FinlandMasala, Finland.

The geometries and topologies of leaves, flowers, roots, shoots, and their arrangements have fascinated plant biologists and mathematicians alike. As such, plant morphology is inherently mathematical in that it describes plant form and architecture with geometrical and topological techniques. Gaining an understanding of how to modify plant morphology, through molecular biology and breeding, aided by a mathematical perspective, is critical to improving agriculture, and the monitoring of ecosystems is vital to modeling a future with fewer natural resources. In this white paper, we begin with an overview in quantifying the form of plants and mathematical models of patterning in plants. We then explore the fundamental challenges that remain unanswered concerning plant morphology, from the barriers preventing the prediction of phenotype from genotype to modeling the movement of leaves in air streams. We end with a discussion concerning the education of plant morphology synthesizing biological and mathematical approaches and ways to facilitate research advances through outreach, cross-disciplinary training, and open science. Unleashing the potential of geometric and topological approaches in the plant sciences promises to transform our understanding of both plants and mathematics.
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http://dx.doi.org/10.3389/fpls.2017.00900DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5465304PMC
June 2017

Morphometric analysis of Passiflora leaves: the relationship between landmarks of the vasculature and elliptical Fourier descriptors of the blade.

Gigascience 2017 01;6(1):1-13

Departamento de Biologia Vegetal/BIOAGRO, Universidade Federal de Viçosa, Viçosa, MG, Brasil.

Background: Leaf shape among Passiflora species is spectacularly diverse. Underlying this diversity in leaf shape are profound changes in the patterning of the primary vasculature and laminar outgrowth. Each of these aspects of leaf morphology-vasculature and blade-provides different insights into leaf patterning.

Results: Here, we morphometrically analyze >3300 leaves from 40 different Passiflora species collected sequentially across the vine. Each leaf is measured in two different ways: using 1) 15 homologous Procrustes-adjusted landmarks of the vasculature, sinuses, and lobes; and 2) Elliptical Fourier Descriptors (EFDs), which quantify the outline of the leaf. The ability of landmarks, EFDs, and both datasets together are compared to determine their relative ability to predict species and node position within the vine. Pairwise correlation of x and y landmark coordinates and EFD harmonic coefficients reveals close associations between traits and insights into the relationship between vasculature and blade patterning.

Conclusions: Landmarks, more reflective of the vasculature, and EFDs, more reflective of the blade contour, describe both similar and distinct features of leaf morphology. Landmarks and EFDs vary in ability to predict species identity and node position in the vine and exhibit a correlational structure (both within landmark or EFD traits and between the two data types) revealing constraints between vascular and blade patterning underlying natural variation in leaf morphology among Passiflora species.
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http://dx.doi.org/10.1093/gigascience/giw008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5437945PMC
January 2017

Persistent homology and the branching topologies of plants.

Am J Bot 2017 03 24;104(3):349-353. Epub 2017 Mar 24.

Donald Danforth Plant Science Center, 975 N. Warson Road, St. Louis, Missouri 63132 USA

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http://dx.doi.org/10.3732/ajb.1700046DOI Listing
March 2017

Gene expression atlas for the food security crop cassava.

New Phytol 2017 Mar 24;213(4):1632-1641. Epub 2017 Jan 24.

Donald Danforth Plant Science Center, 975 North Warson Road, St Louis, MO, 63132, USA.

Cassava (Manihot esculenta) feeds c. 800 million people world-wide. Although this crop displays high productivity under drought and poor soil conditions, it is susceptible to disease, postharvest deterioration and the roots contain low nutritional content. Here, we provide molecular identities for 11 cassava tissue/organ types through RNA-sequencing and develop an open access, web-based interface for further interrogation of the data. Through this dataset, we consider the physiology of cassava. Specifically, we focus on identification of the transcriptional signatures that define the massive, underground storage roots used as a food source and the favored target tissue for transgene integration and genome editing, friable embryogenic callus (FEC). Further, we identify promoters able to drive strong expression in multiple tissue/organs. The information gained from this study is of value for both conventional and biotechnological improvement programs.
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http://dx.doi.org/10.1111/nph.14443DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5516207PMC
March 2017

Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton (Gossypium hirsutum L.).

Proc Natl Acad Sci U S A 2017 01 20;114(1):E57-E66. Epub 2016 Dec 20.

Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC 27695-7620;

Leaf shape varies spectacularly among plants. Leaves are the primary source of photoassimilate in crop plants, and understanding the genetic basis of variation in leaf morphology is critical to improving agricultural productivity. Leaf shape played a unique role in cotton improvement, as breeders have selected for entire and lobed leaf morphs resulting from a single locus, okra (l-D), which is responsible for the major leaf shapes in cotton. The l-D locus is not only of agricultural importance in cotton, but through pioneering chimeric and morphometric studies, it has contributed to fundamental knowledge about leaf development. Here we show that an HD-Zip transcription factor homologous to the LATE MERISTEM IDENTITY1 (LMI1) gene of Arabidopsis is the causal gene underlying the l-D locus. The classical okra leaf shape allele has a 133-bp tandem duplication in the promoter, correlated with elevated expression, whereas an 8-bp deletion in the third exon of the presumed wild-type normal allele causes a frame-shifted and truncated coding sequence. Our results indicate that subokra is the ancestral leaf shape of tetraploid cotton that gave rise to the okra allele and that normal is a derived mutant allele that came to predominate and define the leaf shape of cultivated cotton. Virus-induced gene silencing (VIGS) of the LMI1-like gene in an okra variety was sufficient to induce normal leaf formation. The developmental changes in leaves conferred by this gene are associated with a photosynthetic transcriptomic signature, substantiating its use by breeders to produce a superior cotton ideotype.
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http://dx.doi.org/10.1073/pnas.1613593114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5224360PMC
January 2017

Left-right leaf asymmetry in decussate and distichous phyllotactic systems.

Philos Trans R Soc Lond B Biol Sci 2016 12;371(1710)

Department of Plant Biology, University of California, Davis, CA 95616, USA

Leaves in plants with spiral phyllotaxy exhibit directional asymmetries, such that all the leaves originating from a meristem of a particular chirality are similarly asymmetric relative to each other. Models of auxin flux capable of recapitulating spiral phyllotaxis predict handed auxin asymmetries in initiating leaf primordia with empirically verifiable effects on superficially bilaterally symmetric leaves. Here, we extend a similar analysis of leaf asymmetry to decussate and distichous phyllotaxy. We found that our simulation models of these two patterns predicted mirrored asymmetries in auxin distribution in leaf primordia pairs. To empirically verify the morphological consequences of asymmetric auxin distribution, we analysed the morphology of a tomato sister-of-pin-formed1a (sopin1a) mutant, entire-2, in which spiral phyllotaxy consistently transitions to a decussate state. Shifts in the displacement of leaflets on the left and right sides of entire-2 leaf pairs mirror each other, corroborating predicted model results. We then analyse the shape of more than 800 common ivy (Hedera helix) and more than 3000 grapevine (Vitis and Ampelopsis spp.) leaf pairs and find statistical enrichment of predicted mirrored asymmetries. Our results demonstrate that left-right auxin asymmetries in models of decussate and distichous phyllotaxy successfully predict mirrored asymmetric leaf morphologies in superficially symmetric leaves.This article is part of the themed issue 'Provocative questions in left-right asymmetry'.
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http://dx.doi.org/10.1098/rstb.2015.0412DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5104511PMC
December 2016

A renaissance in plant development.

Dev Biol 2016 Nov 13;419(1):4-6. Epub 2016 Sep 13.

Department of Molecular, Cellular and Developmental Biology, USA; Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA.

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http://dx.doi.org/10.1016/j.ydbio.2016.09.013DOI Listing
November 2016

A sister of PIN1 gene in tomato (Solanum lycopersicum) defines leaf and flower organ initiation patterns by maintaining epidermal auxin flux.

Dev Biol 2016 11 20;419(1):85-98. Epub 2016 Aug 20.

Department of Plant Biology, University of California at Davis, Davis, CA, USA. Electronic address:

The spatiotemporal localization of the plant hormone auxin acts as a positional cue during early leaf and flower organogenesis. One of the main contributors to auxin localization is the auxin efflux carrier PIN-FORMED1 (PIN1). Phylogenetic analysis has revealed that PIN1 genes are split into two sister clades; PIN1 and the relatively uncharacterized Sister-Of-PIN1 (SoPIN1). In this paper we identify entire-2 as a loss-of-function SlSoPIN1a (Solyc10g078370) mutant in Solanum lycopersicum. The entire-2 plants are unable to specify proper leaf initiation leading to a frequent switch from the wild type spiral phyllotactic pattern to distichous and decussate patterns. Leaves in entire-2 are large and less complex and the leaflets display spatial deformities in lamina expansion, vascular development, and margin specification. During sympodial growth in entire-2 the specification of organ position and identity is greatly affected resulting in variable branching patterns on the main sympodial and inflorescence axes. To understand how SlSoPIN1a functions in establishing proper auxin maxima we used the auxin signaling reporter DR5: Venus to visualize differences in auxin localization between entire-2 and wild type. DR5: Venus visualization shows a widening of auxin localization which spreads to subepidermal tissue layers during early leaf and flower organogenesis, showing that SoPIN1 functions to focus auxin signaling to the epidermal layer. The striking spatial deformities observed in entire-2 help provide a mechanistic framework for explaining the function of the SoPIN1 clade in S.lycopersicum.
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http://dx.doi.org/10.1016/j.ydbio.2016.08.011DOI Listing
November 2016

A New Advanced Backcross Tomato Population Enables High Resolution Leaf QTL Mapping and Gene Identification.

G3 (Bethesda) 2016 10 13;6(10):3169-3184. Epub 2016 Oct 13.

Department of Plant Biology, University of California at Davis, California 95616

Quantitative Trait Loci (QTL) mapping is a powerful technique for dissecting the genetic basis of traits and species differences. Established tomato mapping populations between domesticated tomato (Solanum lycopersicum) and its more distant interfertile relatives typically follow a near isogenic line (NIL) design, such as the S. pennellii Introgression Line (IL) population, with a single wild introgression per line in an otherwise domesticated genetic background. Here, we report on a new advanced backcross QTL mapping resource for tomato, derived from a cross between the M82 tomato cultivar and S. pennellii This so-called Backcrossed Inbred Line (BIL) population is comprised of a mix of BC and BC lines, with domesticated tomato as the recurrent parent. The BIL population is complementary to the existing S. pennellii IL population, with which it shares parents. Using the BILs, we mapped traits for leaf complexity, leaflet shape, and flowering time. We demonstrate the utility of the BILs for fine-mapping QTL, particularly QTL initially mapped in the ILs, by fine-mapping several QTL to single or few candidate genes. Moreover, we confirm the value of a backcrossed population with multiple introgressions per line, such as the BILs, for epistatic QTL mapping. Our work was further enabled by the development of our own statistical inference and visualization tools, namely a heterogeneous hidden Markov model for genotyping the lines, and by using state-of-the-art sparse regression techniques for QTL mapping.
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http://dx.doi.org/10.1534/g3.116.030536DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5068939PMC
October 2016

eQTL Regulating Transcript Levels Associated with Diverse Biological Processes in Tomato.

Plant Physiol 2016 09 14;172(1):328-40. Epub 2016 Jul 14.

Department of Plant Biology, University of California, Davis, California 95616

Variation in gene expression, in addition to sequence polymorphisms, is known to influence developmental, physiological, and metabolic traits in plants. Genetic mapping populations have facilitated identification of expression quantitative trait loci (eQTL), the genetic determinants of variation in gene expression patterns. We used an introgression population developed from the wild desert-adapted Solanum pennellii and domesticated tomato (Solanum lycopersicum) to identify the genetic basis of transcript level variation. We established the effect of each introgression on the transcriptome and identified approximately 7,200 eQTL regulating the steady-state transcript levels of 5,300 genes. Barnes-Hut t-distributed stochastic neighbor embedding clustering identified 42 modules revealing novel associations between transcript level patterns and biological processes. The results showed a complex genetic architecture of global transcript abundance pattern in tomato. Several genetic hot spots regulating a large number of transcript level patterns relating to diverse biological processes such as plant defense and photosynthesis were identified. Important eQTL regulating transcript level patterns were related to leaf number and complexity as well as hypocotyl length. Genes associated with leaf development showed an inverse correlation with photosynthetic gene expression, but eQTL regulating genes associated with leaf development and photosynthesis were dispersed across the genome. This comprehensive eQTL analysis details the influence of these loci on plant phenotypes and will be a valuable community resource for investigations on the genetic effects of eQTL on phenotypic traits in tomato.
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http://dx.doi.org/10.1104/pp.16.00289DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5074602PMC
September 2016
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