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Research ArticleArticle
Open Access

A Modern Ampelography: A Genetic Basis for Leaf Shape and Venation Patterning in Grape

Daniel H. Chitwood, Aashish Ranjan, Ciera C. Martinez, Lauren R. Headland, Thinh Thiem, Ravi Kumar, Michael F. Covington, Tommy Hatcher, Daniel T. Naylor, Sharon Zimmerman, Nora Downs, Nataly Raymundo, Edward S. Buckler, Julin N. Maloof, Mallikarjuna Aradhya, Bernard Prins, Lin Li, Sean Myles, Neelima R. Sinha
Daniel H. Chitwood
Department of Plant Biology (D.H.C., A.R., C.C.M., L.R.H., T.T., R.K., M.F.C., T.H., D.T.N., S.Z., N.D., N.R., J.N.M., N.R.S.) and National Clonal Germplasm Repository, United States Department of Agriculture-Agricultural Research Service (M.A., B.P.), University of California, Davis, California 95616
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  • ORCID record for Daniel H. Chitwood
Aashish Ranjan
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Ciera C. Martinez
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Lauren R. Headland
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Thinh Thiem
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Ravi Kumar
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Michael F. Covington
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Tommy Hatcher
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Daniel T. Naylor
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Sharon Zimmerman
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Nora Downs
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Nataly Raymundo
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Edward S. Buckler
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Julin N. Maloof
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Mallikarjuna Aradhya
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Bernard Prins
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Lin Li
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Sean Myles
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Neelima R. Sinha
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  • For correspondence: nrsinha@ucdavis.edu

Published January 2014. DOI: https://doi.org/10.1104/pp.113.229708

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  • Figure 1.
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    Figure 1.

    AR and circularity among grape accessions. Averaged AR (major/minor axis of a fitted ellipse) and circularity (the ratio of area to perimeter squared times 4π) values of 1,213 accessions in the USDA germplasm collection are shown. In this population, high AR values indicate leaves with low length-to-width ratios, and leaves with low circularity have increased lobing and serration. Leaves from accessions exhibiting extreme AR and circularity values are shown. In this and subsequent figures, the common name (boldface), place of origin (italics), and accession number (roman) of leaves is provided below the photographs. [See online article for color version of this figure.]

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    Figure 2.

    EFDs of symmetrical shape variation. Eigenleaves resulting from a PCA on EFDs derived from 9,485 leaves of 1,220 accessions are shown. Shown are the first five PCs and the percentage variation in symmetrical shape that they explain. For each PC, the eigenleaves at −2 (blue) and +2 (orange) sd along the PC axis are shown. An overlay of the eigenleaves at ±2 sd indicates the shape variance explained by each PC. Representative leaves of accessions with extreme PC values are shown. PCs resulting from the analysis of EFDs are indicated as symPC, referring to the symmetrical shape variance they explain. The five symPCs considered in this article explain 84.4% of all symmetrical shape variance analyzed.

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    Figure 3.

    GPA of venation patterning. A, PCs resulting from a Procrustes analysis of “outer landmarks” (these PCs are indicated as oPCs). There are 10 landmarks in the outer analysis, including the petiolar junction, tip of the midrib (L1), the tips of the left and right superior (distal; L2) and inferior (proximal; L3) lobes, and the left and right superior (Sis) and inferior (Sii) sinuses. For each PC, eigenleaves at −2 (blue) and +2 (orange) sd along the PC axis, the overlay of these leaves, and the percentage variation explained by the PC are given. Representative leaves from accessions with extreme values for each PC are shown. The three PCs analyzed in the outer analysis explain 63.5% of the variance in this data set. B, Similar to A, except showing PCs resulting from analysis of the “inner landmarks.” There are six landmarks in the inner analysis, including the petiolar junction, branch point of the midrib (L1), the left and right major branch points of the superior (L2) lateral veins, and the left and right branch points between the inferior (L3) and petiolar (L4) veins. The three PCs analyzed in the inner analysis explain 75.8% of the variance in this data set. For visual descriptions of the midrib (L1), superior lateral veins (L2), inferior lateral veins (L3), petiolar veins (L4), and superior and inferior sinuses (Sis and Sii), see Figure 4B.

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    Figure 4.

    Correlation of traits with each other and with measurements from Galet (1952). A, Hierarchical clustering and heat map of the correlation of traits, as measured in 1,220 accessions, with each other. The top quadrant indicates correlation P values, and the bottom quadrant indicates Spearman’s ρ. The solid line box indicates high correlation between symPC1, circularity, and oPC1, traits related to lobing and serration. The dashed line box indicates high correlation between symPC3, iPC3, oPC2, AR, iPC1, and symPC4, measures that are sensitive to the angular placement of the superior and inferior lateral veins to each other. B, Traits measured by Galet (1952, 1979). Measures of vein length (L1–L4), sinus distance (Sis and Sii), and angles between veins (∠S and ∠S′) are indicated and defined. r is length-to-width ratio; A, B, and C are ratios of vein lengths; S and S′ are angular distances between veins; and low/highSup and low/highInf are low and high estimates of superior and inferior lobing. C, Hierarchical clustering and heat map of the correlation of traits measured in this article with that of Galet (1952; indicated in light gray in the margins). Correlation is between 122 accessions matched between the USDA germplasm collection and Galet (1952). The solid line box indicates high correlation between the measures of Galet (1952) for lobing and measures of lobing and serration measured in this article. The dashed line box indicates high correlation between the measures of Galet (1952) for angular positioning of superior and inferior veins with similar traits measured in the USDA germplasm collection. P values are indicated in orange to purple (less to more significant) and gray (not significant [NS/NA]). Spearman’s ρ is indicated in blue (negative), yellow (positive), and white (neutral).

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    Figure 5.

    Meta-analysis of traits with data from GRIN. A, Hierarchical clustering and heat map of the correlation of traits with those present in GRIN. Seventy-five GRIN traits (representing 36 distinct phenotypes measured in multiple years at the USDA germplasm collection) are hierarchically clustered with traits measured in this article. Most traits measured in this article (black rectangles) cluster together (gray box). P values are indicated in orange to purple (less to more significant) and gray (not significant, [NS/NA]). r is length-to-width ratio, indicated in blue (negative), yellow (positive), and white (neutral). B, Closeup of the gray box in A. Traits relating to the angular placement of the superior and inferior veins correlate most closely with trichome density (LEAF_HAIR and SHOOT_HAIR) and shape of the petiolar sinus (PETSINMALF). C and D, Significant correlations of AR (C) and iPC3 (D) with GRIN leaf and shoot trichome densities shown as box plots superimposed upon jittered values. FDR-controlled P values for correlations are provided.

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    Figure 6.

    Population structure of grape and V. sylvestris accessions. PCA results reflect the population structure in wild and domesticated grape. Genotypic PCs are referred to as genoPCs to distinguish them from other trait PCs used in this article. Graphs of genoPC1 and genoPC3 (explaining 6.35% and 2.31% of genotypic variation, respectively) with grape accessions colored by point of origin (A; western, black; central, orange; eastern, magenta) and by production type (B; wine, blue; table, yellow) are shown. In both graphs, western and eastern V. sylvestris accessions are indicated by black and magenta, respectively. genoPC1 and genoPC3 are shown because of their prominent correlations with traits. Note that genoPC1 explains the eastern versus western population structure, whereas genoPC3 explains the central-specific patterns of variance. The V. sylvestris accession DVIT2426 that was sampled is indicated.

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    Figure 7.

    Correlations between traits and genotypic PCs. A, Box plots of significant correlations between genoPC1 and genoPC3 with GRIN measures of trichome density and leaf circularity. Bonferroni-corrected P values are provided. B to G, iPC3 (B–D) and AR (E–G) are two traits that correlate not only with genoPCs (genoPC1 and genoPC3, respectively) but also with production type and geographical attributes of accessions (iPC3 with production type and AR with geography). For genoPC1/iPC3 and genoPC3/AR, correlations between the genoPC and trait are provided, as well as differences by production type and geography as a box plot, and a colored map indicates average trait values for accessions by country of origin. Note that for iPC3, the Tunisian accession sampled (DVIT2426; indicated by asterisks in the box plots and maps) has trait values resembling those for wine grapes, which predominately occupy western Europe near Tunisia. iPC3 values decrease West to East, reflecting the correlation with genoPC1. Similarly, the AR of the Tunisian accession’s leaves resembles that of western cultivars, and the lowest ARs are found in leaves from central accessions, reflecting the central-specific pattern of genotypic variance explained by genoPC3 with which AR correlates.

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    Figure 8.

    GWAS mapping of leaf traits. A, Significant associations between genetic markers measured by Myles et al. (2011) and leaf traits as determined using EMMAX (Kang et al., 2008) are shown. Negative log-transformed P values, indicated in blue and green for alternating chromosomes, are shown across the length of the genome with a Bonferroni-corrected P value threshold (0.05) indicated as a dotted red line. oPC1 and circularity significantly associate with the same polymorphism on chromosome 1. iPC3 associates with a nearby marker on chromosome 1, and iPC2 associates with a marker on chromosome 6. B, Expanded view of the yellow highlighted regions in A, showing significantly associated markers with iPC3, oPC1, and circularity on chromosome 1 (blue lines). Orange lines indicate homologs regulating leaf development within 2 Mb in either direction (names in gray below graph). Positions of differentially expressed genes between Chasselas Ciotat and Chasselas Dore and their log2 fold change values (y axis) are indicated by points (size proportional to significance). C, Similar to B, showing the expanded view of the pink highlighted region in A for the SNP associated with iPC2.

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    Table I. Heritability estimates of traits

    Estimates of the heritability of traits accounting for population structure and cryptic relatedness are as described by Yang et al. (2011). Provided are the trait, sample number, and heritability estimate.

    Traitnh2
    oPC29280.4594
    symPC19360.4321
    symPC49360.4285
    oPC19260.4222
    iPC39280.4184
    iPC19280.4064
    Circularity9270.3949
    iPC29280.3936
    symPC59360.3415
    symPC39360.3144
    oPC39280.2303
    AR9280.2277
    symPC29340.2162

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    Supplemental Figure, Tables, and Data

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    • Supplemental Data - Supplemental Data 8
    • Supplemental Data - Supplemental Data 5
    • Supplemental Data - Supplemental Figure 1
    • Supplemental Data - Supplemental Data 16
    • Supplemental Data - Supplemental Data 18
    • Supplemental Data - Supplemental Data 14
    • Supplemental Data - Supplemental Data 12
    • Supplemental Data - Supplemental Data 6
    • Supplemental Data - Supplemental Data 11
    • Supplemental Data - Supplemental Table 1
    • Supplemental Data - Supplemental Table 2
    • Supplemental Data - Supplemental Data 2
    • Supplemental Data - Supplemental Data 19
    • Supplemental Data - Supplemental Data 13
    • Supplemental Data - Supplemental Data 17
    • Supplemental Data - Supplemental Data 9
    • Supplemental Data - Supplemental Data 1
    • Supplemental Data - Supplemental Data 10
    • Supplemental Data - Supplemental Data 4
    • Supplemental Data - Supplemental Data 15
    • Supplemental Data - Supplemental Data 7
    • Supplemental Data - Supplemental Data 3

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A Modern Ampelography: A Genetic Basis for Leaf Shape and Venation Patterning in Grape
Daniel H. Chitwood, Aashish Ranjan, Ciera C. Martinez, Lauren R. Headland, Thinh Thiem, Ravi Kumar, Michael F. Covington, Tommy Hatcher, Daniel T. Naylor, Sharon Zimmerman, Nora Downs, Nataly Raymundo, Edward S. Buckler, Julin N. Maloof, Mallikarjuna Aradhya, Bernard Prins, Lin Li, Sean Myles, Neelima R. Sinha
Plant Physiology Jan 2014, 164 (1) 259-272; DOI: 10.1104/pp.113.229708

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A Modern Ampelography: A Genetic Basis for Leaf Shape and Venation Patterning in Grape
Daniel H. Chitwood, Aashish Ranjan, Ciera C. Martinez, Lauren R. Headland, Thinh Thiem, Ravi Kumar, Michael F. Covington, Tommy Hatcher, Daniel T. Naylor, Sharon Zimmerman, Nora Downs, Nataly Raymundo, Edward S. Buckler, Julin N. Maloof, Mallikarjuna Aradhya, Bernard Prins, Lin Li, Sean Myles, Neelima R. Sinha
Plant Physiology Jan 2014, 164 (1) 259-272; DOI: 10.1104/pp.113.229708
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