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      The tomato genome sequence provides insights into fleshy fruit evolution

      The Tomato Genome Consortium (TGC)

      Nature

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          Abstract

          Introductory Paragraph Tomato (Solanum lycopersicum) is a major crop plant and a model system for fruit development. Solanum is one of the largest angiosperm genera 1 and includes annual and perennial plants from diverse habitats. We present a high quality genome sequence of domesticated tomato, a draft sequence of its closest wild relative, S. pimpinellifolium 2 , and compare them to each other and to potato (S. tuberosum). The two tomato genomes show only 0.6% nucleotide divergence and signs of recent admixture, but show >8% divergence from potato, with nine large and several smaller inversions. In contrast to Arabidopsis, but similar to soybean, tomato and potato, small RNAs map predominantly to gene-rich chromosomal regions, including gene promoters. The Solanum lineage has experienced two consecutive genome triplications: one that is ancient and shared with rosids, and a more recent one. These triplications set the stage for the neofunctionalization of genes controlling fruit characteristics, such as colour and fleshiness. Main Text The genome of the inbred tomato cultivar ‘Heinz 1706’ was sequenced and assembled using a combination of Sanger and “next generation” technologies (Supplementary Section 1). The predicted genome size is ~900 Mb, consistent with prior estimates 3 , of which 760 Mb were assembled in 91 scaffolds aligned to the 12 tomato chromosomes, with most gaps restricted to pericentromeric regions (Fig. 1A; Supplementary Fig. 1). Base accuracy is approximately one substitution error per 29.4 kb and one indel error per 6.4 kb. The scaffolds were linked with two BAC-based physical maps and anchored/oriented using a high-density genetic map, introgression line mapping and BAC fluorescence in situ hybridisation (FISH). The genome of S. pimpinellifolium (accession LA1589) was sequenced and assembled de novo using Illumina short reads, yielding a 739 Mb draft genome (Supplementary Section 3). Estimated divergence between the wild and domesticated genomes is 0.6% (5.4M SNPs distributed along the chromosomes (Fig. 1A, Supplementary Fig. 1)). Tomato chromosomes consist of pericentric heterochromatin and distal euchromatin, with repeats concentrated within and around centromeres, in chromomeres and at telomeres (Fig. 1A, Supplementary Fig. 1). Substantially higher densities of recombination, genes and transcripts are observed in euchromatin, while chloroplast insertions (Supplementary Sections 1.22-1.23) and conserved miRNA genes (Supplementary Section 2.9) are more evenly distributed throughout the genome. The genome is highly syntenic with those of other economically important Solanaceae (Fig. 1B). Compared to the genomes of Arabidopsis 4 and sorghum 5 , tomato has fewer high-copy, full-length LTR retrotransposons with older average insertion ages (2.8 versus 0.8 mya) and fewer high-frequency k-mers (Supplementary Section 2.10). This supports previous findings that the tomato genome is unusual among angiosperms by being largely comprised of low-copy DNA 6,7 . The pipeline used to annotate the tomato and potato 8 genomes is described in Supplementary Section 2. It predicted 34,727 and 35,004 protein-coding genes, respectively. Of these, 30,855 and 32,988, respectively, are supported by RNA-Seq data, and 31,741 and 32,056, respectively, show high similarity to Arabidopsis genes (Supplementary section 2.1). Chromosomal organisation of genes, transcripts, repeats and sRNAs is very similar in the two species (Supplementary Figures 2-4). The protein coding genes of tomato, potato, Arabidopsis, rice and grape were clustered into 23,208 gene groups (≥2 members), of which 8,615 are common to all five genomes, 1,727 are confined to eudicots (tomato, potato, grape and Arabidopsis), and 727 are confined to plants with fleshy fruits (tomato, potato and grape) (Supplementary Section 5.1, Supplementary Fig. 5). Relative expression of all tomato genes was determined by replicated strand-specific Illumina RNA-Seq of root, leaf, flower (2 stages) and fruit (6 stages) in addition to leaf and fruit (3 stages) of S. pimpinellifolium (Supplementary Table 1). sRNA sequencing data supported the prediction of 96 conserved miRNA genes in tomato and 120 in potato, a number consistent with other plant species (Fig. 1A, Supplementary Figures 1 and 3, Supplementary Section 2.9). Among the 34 miRNA families identified, 10 are highly conserved in plants and similarly represented in the two species, whereas other, less conserved families are more abundant in potato. Several miRNAs, predicted to target TIR-NBS-LRR genes, appeared to be preferentially or exclusively expressed in potato (Supplementary Section 2.9). Supplementary section 4 deals with comparative genomic studies. Sequence alignment of 71 Mb of euchromatic tomato genomic DNA to their potato 8 counterparts revealed 8.7% nucleotide divergence (Supplementary Section 4.1). Intergenic and repeat-rich heterochromatic sequences showed more than 30% nucleotide divergence, consistent with the high sequence diversity in these regions among potato genotypes 8 . Alignment of tomato-potato orthologous regions confirmed 9 large inversions known from cytological or genetic studies and several smaller ones (Fig. 1C). The exact number of small inversions is difficult to determine due to the lack of orientation of most potato scaffolds. 18,320 clearly orthologous tomato-potato gene pairs were identified. Of these, 138 (0.75%) had significantly higher than average non-synonymous (Ka) versus synonymous (Ks) nucleotide substitution rate ratios (ω), suggesting diversifying selection, whereas 147 (0.80%) had significantly lower than average ω, suggesting purifying selection (Supplementary Table 2). The proportions of high and low ω between sorghum and maize (Zea mays) are 0.70% and 1.19%, respectively, after 11.9 Myr of divergence 9 , suggesting that diversifying selection may have been stronger in tomato-potato. The highest densities of low-ω genes are found in collinear blocks with average Ks >1.5, tracing to a genome triplication shared with grape (see below) (Fig. 1C, Supplementary Fig. 6, Supplementary Table 3). These genes, which have been preserved in paleo-duplicated locations for more than 100 Myr 10,11 are more constrained than ‘average’ genes and are enriched for transcription factors and genes otherwise related to gene regulation (Supplementary Tables 3-4). Sequence comparison of 32,955 annotated genes in tomato and S. pimpinellifolium revealed 6,659 identical genes and 3,730 with only synonymous changes. A total of 22,888 genes had non-synonymous changes, including gains and losses of stop codons with potential consequences for gene function (Supplementary Tables 5-7). Several pericentric regions, predicted to contain genes, are absent or polymorphic in the broader S. pimpinellifolium germplasm (Supplementary Table 8, Supplementary Fig. 7). Within cultivated germplasm, particularly among the small-fruited cherry tomatoes, several chromosomal segments are more closely related to S. pimpinellifolium than to ‘Heinz 1706’ (Supplementary Figures 8-9), supporting previous observations on recent admixture of these gene pools due to breeding 12 . ‘Heinz 1706’ itself has been reported to carry introgressions from S. pimpinellifolium 13 , traces of which are detectable on chromosomes 4, 9, 11 and 12 (Supplementary Table 9). Comparison of the tomato and grape genomes supports the hypothesis that a whole-genome triplication affecting the rosid lineage occurred in a common eudicot ancestor 11 (Fig. 2B). The distribution of Ks between corresponding gene pairs in duplicated blocks suggests that one polyploidisation in the solanaceous lineage preceded the rosid-asterid (tomato-grape) divergence (Supplementary Fig. 10). Comparison to the grape genome also reveals a more recent triplication in tomato and potato. While few individual tomato/potato genes remain triplicated (Supplementary Tables 10-11), 73% of tomato gene models are in blocks that are orthologous to one grape region, collectively covering 84% of the grape gene space. Among these grape genomic regions, 22.5% have one orthologous region in tomato, 39.9% have two, and 21.6% have three, indicating that a whole genome triplication occurred in the Solanum lineage, followed by widespread gene loss. This triplication, also evident in potato (Supplementary Fig. 11) is estimated at 71 (+/-19.4) mya based on Ks of paralogous genes (Supplementary Fig. 10), and therefore predates the ~7.3 mya tomato-potato divergence. Based on alignments to single grape genome segments, the tomato genome can be partitioned into three non-overlapping ‘subgenomes’ (Fig. 2A). The number of euasterid lineages that have experienced the recent triplication remains unclear and awaits complete euasterid I and II genome sequences. Ks distributions show that euasterids I and II, and indeed the rosid-asterid lineages, all diverged from common ancestry at or near the pan-eudicot triplication (Fig. 2B), suggesting that this event may have contributed to formation of major eudicot lineages in a short period of several million years 14 , partially explaining the explosive radiation of angiosperm plants on earth 15 . Supplementary section 5 reports on the analysis of specific gene families. Fleshy fruits (Supplementary Fig. 12) are an important means of attracting vertebrate frugivores for seed dispersal 16 . Combined orthology and synteny analyses suggest that both genome triplications added new gene family members that mediate important fruit-specific functions (Fig. 3). These include transcription factors and enzymes necessary for ethylene biosynthesis (RIN, CNR, ACS) and perception (LeETR3/NR, LeETR4) 17 , red light photoreceptors influencing fruit quality (PHYB1/PHYB2) and ethylene- and light-regulated genes mediating lycopene biosynthesis (PSY1/PSY2). Several cytochrome P450 subfamilies associated with toxic alkaloid biosynthesis show contraction or complete loss in tomato and the extant genes show negligible expression in ripe fruits (Supplementary Section 5.4). Fruit texture has profound agronomic and sensory importance and is controlled in part by cell wall structure and composition 18 . More than 50 genes showing differential expression during fruit development and ripening encode proteins involved in modification of wall architecture (Fig. 4A and Supplementary Section 5.7). For example, a family of xyloglucan endotransglucosylase-/hydrolases (XTHs) has expanded both in the recent whole genome triplication and through tandem duplication. One of the triplicated members, SlXTH10, shows differential loss between tomato and potato (Fig. 4A, Supplementary Table 12), suggesting genetically driven specialisation in the remodelling of fruit cell walls. Similar to soybean and potato and in contrast to Arabidopsis, tomato sRNAs map preferentially to euchromatin (Supplementary Fig. 2). sRNAs from tomato flowers and fruits 19 map to 8,416 gene promoters. Differential expression of sRNAs during fruit development is apparent for 2,687 promoters, including those of cell wall-related genes (Fig. 4B) and occurs preferentially at key developmental transitions (e.g. flower to fruit, fruit growth to fruit ripening, Supplementary Section 2.8). The genome sequences of tomato, S. pimpinellifolium and potato provide a starting point for comparing gene family evolution and sub-functionalization in the Solanaceae. A striking example is the SELF PRUNING (SP) gene family, which includes the homolog of Arabidopsis FT, encoding the mobile flowering hormone florigen 20 and its antagonist SP, encoding the ortholog of TFL1. Nearly a century ago, a spontaneous mutation in SP spawned the “determinate” varieties that now dominate the tomato mechanical harvesting industry 21 . The genome sequence has revealed that the SP family has expanded in the Solanum lineage compared to Arabidopsis, driven by the Solanum triplication and tandem duplication (Supplementary Fig. 13). In potato, SP3D and SP6A control flowering and tuberisation, respectively 22 , whereas SP3D in tomato, known as SINGLE FLOWER TRUSS, similarly controls flowering, but also drives heterosis for fruit yield in an epistatic relationship with SP 23,24,25 . Interestingly, SP6A in S. lycopersicum is inactivated by a premature stop codon, but remains functionally intact in S. pimpinellifolium. Thus, allelic variation in a subset of SP family genes has played a major role in the generation of both shared and species-specific variation in Solanaceous agricultural traits. The genome sequences of tomato and S. pimpinellifolium also provide a basis for understanding the bottlenecks that have narrowed tomato genetic diversity: the domestication of S. pimpinellifolium in the Americas, the export of a small number of accessions to Europe in the 16th Century, and the intensive breeding that followed. Charles Rick pioneered the use of trait introgression from wild tomato relatives to increase genetic diversity of cultivated tomatoes 26 . Introgression lines exist for seven wild tomato species, including S. pimpinellifolium, in the background of cultivated tomato. The genome sequences presented here and the availability of millions of SNPs will allow breeders to revisit this rich trait reservoir and identify domestication genes, providing biological knowledge and empowering biodiversity-based breeding. Methods Summary A total of 21 Gb of Roche/454 Titanium shotgun and matepair reads and 3.3 Gb of Sanger paired-end reads, including ~200,000 BAC and fosmid end sequence pairs, were generated from the ‘Heinz 1706’ inbred line (Supplementary Sections 1.1-1.7), assembled using both Newbler and CABOG and integrated into a single assembly (Supplementary Sections 1.17-1.18). The scaffolds were anchored using two BAC-based physical maps, one high density genetic map, overgo hybridization and genome-wide BAC FISH (Supplementary Sections 1.8-1.16 and 1.19). Over 99.9% of BAC/fosmid end pairs mapped consistently on the assembly and over 98% of EST sequences could be aligned to the assembly (Supplementary Section 1.20). Chloroplast genome insertions in the nuclear genome were validated using a matepair method and the flanking regions were identified (Supplementary Sections 1.22-1.24). Annotation was carried out using a pipeline based on EuGene that integrates de novo gene prediction, RNA-Seq alignment and rich function annotation (Supplementary Section 2). To facilitate interspecies comparison, the potato genome was re-annotated using the same pipeline. LTR retrotransposons were detected de novo with the LTR-STRUC program and dated by the sequence divergence between left and right solo LTR (Supplementary Section 2.10). The genome of S. pimpinellifolium was sequenced to 40x depth using Illumina paired end reads and assembled using ABySS (Supplementary Section 3). The tomato and potato genomes were aligned using LASTZ (Supplementary Section 4.1). Identification of triplicated regions was done using BLASTP, in-house generated scripts and three way comparisons between tomato, potato and S. pimpinellifolium using MCscan (Supplementary Sections 4.2-4.4). Specific gene families/groups (genes for ascorbate, carotenoid and jasmonate biosynthesis, cytochrome P450s, genes controlling cell wall architecture, hormonal and transcriptional regulators, resistance genes) were subjected to expert curation/analysis, (Supplementary Section 5). PHYML and MEGA were used to reconstruct phylogenetic trees and MCSCAN was used to infer gene collinearity (Supplementary Section 5.2). Supplementary Material 1 2 3 4

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          Most cited references 32

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          The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla.

          The analysis of the first plant genomes provided unexpected evidence for genome duplication events in species that had previously been considered as true diploids on the basis of their genetics. These polyploidization events may have had important consequences in plant evolution, in particular for species radiation and adaptation and for the modulation of functional capacities. Here we report a high-quality draft of the genome sequence of grapevine (Vitis vinifera) obtained from a highly homozygous genotype. The draft sequence of the grapevine genome is the fourth one produced so far for flowering plants, the second for a woody species and the first for a fruit crop (cultivated for both fruit and beverage). Grapevine was selected because of its important place in the cultural heritage of humanity beginning during the Neolithic period. Several large expansions of gene families with roles in aromatic features are observed. The grapevine genome has not undergone recent genome duplication, thus enabling the discovery of ancestral traits and features of the genetic organization of flowering plants. This analysis reveals the contribution of three ancestral genomes to the grapevine haploid content. This ancestral arrangement is common to many dicotyledonous plants but is absent from the genome of rice, which is a monocotyledon. Furthermore, we explain the chronology of previously described whole-genome duplication events in the evolution of flowering plants.
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            The Sorghum bicolor genome and the diversification of grasses.

            Sorghum, an African grass related to sugar cane and maize, is grown for food, feed, fibre and fuel. We present an initial analysis of the approximately 730-megabase Sorghum bicolor (L.) Moench genome, placing approximately 98% of genes in their chromosomal context using whole-genome shotgun sequence validated by genetic, physical and syntenic information. Genetic recombination is largely confined to about one-third of the sorghum genome with gene order and density similar to those of rice. Retrotransposon accumulation in recombinationally recalcitrant heterochromatin explains the approximately 75% larger genome size of sorghum compared with rice. Although gene and repetitive DNA distributions have been preserved since palaeopolyploidization approximately 70 million years ago, most duplicated gene sets lost one member before the sorghum-rice divergence. Concerted evolution makes one duplicated chromosomal segment appear to be only a few million years old. About 24% of genes are grass-specific and 7% are sorghum-specific. Recent gene and microRNA duplications may contribute to sorghum's drought tolerance.
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              Synteny and collinearity in plant genomes.

              Correlated gene arrangements among taxa provide a valuable framework for inference of shared ancestry of genes and for the utilization of findings from model organisms to study less-well-understood systems. In angiosperms, comparisons of gene arrangements are complicated by recurring polyploidy and extensive genome rearrangement. New genome sequences and improved analytical approaches are clarifying angiosperm evolution and revealing patterns of differential gene loss after genome duplication and differential gene retention associated with evolution of some morphological complexity. Because of variability in DNA substitution rates among taxa and genes, deviation from collinearity might be a more reliable phylogenetic character.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                23 April 2012
                30 May 2012
                30 November 2012
                : 485
                : 7400
                : 635-641
                Affiliations
                [1 ] Kazusa DNA Research Institute, 2-6-7 Kazusa-kamatari, Kisarazu, Chiba 292-0818, Japan
                [2 ] 454 Life Sciences, a Roche company, 15 Commercial Street, Branford, CT 06405, USA
                [3 ] Amplicon Express Inc., 2345 Hopkins Court, Pullman, WA 99163, USA
                [4 ] Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
                [5 ] BGI-Shenzhen, Shenzhen 518083, China
                [6 ] BMR-Genomics SrL, via Redipuglia 21/A, 35131 Padova, Italy
                [7 ] Boyce Thompson Institute for Plant Research, Tower Road, Cornell University campus, Ithaca, NY 14853, USA
                [8 ] Centre for BioSystems Genomics, PO Box 98, 6700 AB Wageningen, The Netherlands
                [9 ] Centro Nacional de Análisis Genómico (CNAG) and National Bioinformatics Institute, C/ Baldiri Reixac 4, Torre I, 08028 Barcelona, Spain
                [10 ] Genome Bioinformatics Laboratory Center for Genomic Regulation, Dr Aiguader, 88, E-08003 Barcelona, Spain
                [11 ] Department of Vegetable Science, College of Agronomy and Biotechnology, China Agricultural University, No. 2 Yuanmingyuan Xi Lu, Haidian District, Beijing 100193, China
                [12 ] Key Laboratory of Horticultural Crops Genetic Improvement of Ministry of Agriculture, Sino-Dutch Joint Lab of Horticultural Genomics Technology, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China
                [13 ] State Key Laboratory of Plant Genomics and National Centre for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
                [14 ] National Center for Gene Research, Chinese Academy of Sciences, Shanghai 200233, China
                [15 ] Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China
                [16 ] State Key Laboratory of Plant Cell and Chromosome Engineering and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
                [17 ] Laboratory of Molecular and Developmental Biology and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, China
                [18 ] Cold Spring Harbor Laboratory, One Bungtown Road, Cold Spring Harbor, NY 11724, USA
                [19 ] Department of Biology, Colorado State University, Fort Collins, CO 80523, USA
                [20 ] Department of Agronomy, National Taiwan University, Taipei, Taiwan
                [21 ] Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA
                [22 ] Genome Bioinformatics Laboratory; Center for Genomic Regulation (CRG), University Pompeu Fabra, Barcelona, Catalonia, 08003, Spain
                [23 ] Department of Plant Systems Biology, VIB; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, 9052 Gent, Belgium
                [24 ] Faculty of Agriculture, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel
                [25 ] Institute of Industrial Crops, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, China
                [26 ] Institute for Bioinformatics and Systems Biology (MIPS), Helmholtz Center for Health and Environment, Ingolstädter Landstr. 1, D-85764 Neuherberg, Germany
                [27 ] College of Horticulture, Henan Agricultural University, Zhengzhou 450002, China
                [28 ] National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China.
                [29 ] Department of Life Sciences, Imperial College London, London SW7 1AZ, UK
                [30 ] NRC on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, 110 012, India
                [31 ] INRA, UR1052 Génétique et amélioration des fruits et légumes, BP 94, 84143 Monfavet CEDEX, France
                [32 ] INRA, Biologie du Fruit et Pathologie, 71 rue E. Bourleaux, 33883 Villenave d’Ornon, France
                [33 ] Unité de Biométrie et d’Intelligence Artificielle UR 875, INRA, F-31320, Castanet Tolosan, France
                [34 ] INRA-CNRGV BP52627 31326 Castanet-Tolosan, France
                [35 ] Plateforme bioinformatique Genotoul, UR875 Biométrie et Intelligence Artificielle, INRA, 31326 Castanet-Tolosan, France
                [36 ] ENSAT, Avenue de l’Agrobiopole BP 32607 31326 Castanet-Tolosan, France
                [37 ] Instituto de Biología Molecular y Celular de Plantas (CSIC-UPV), Ciudad Politecnica de la Innovación, escalera 8E, Ingeniero Fausto Elios s/n, 46022 Valencia, Spain
                [38 ] Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora”, Universidad de Malaga - Consejo Superior de Investigaciones Cientificas (IHSM-UMA-CSIC), 29750 Algarrobo-Costa (Málaga), Spain
                [39 ] Instituto Nacional de Tecnología Agropecuaría (IB-INTA) and Consejo Nacionalde Investigaciones Científicas y Técnicas (CONICET):; Instituto de Biotecnología, PO Box 25, B1712WAA Castelar, Argentina
                [40 ] Institute for Biomedical Technologies, National Research Council of Italy, Via F. Cervi 93, 20090 Segrate (Milano), Italy
                [41 ] Institute of Plant Genetics, Research Division Portici, National Research Council of Italy, Via Università 133, 80055 Portici, Italy
                [42 ] Italian National Agency for New technologies, Energy and Sustainable Development:; ENEA, Casaccia Research Center, Via Anguillarese 301, 00123 Roma, Italy
                [43 ] Scuola Superiore Sant’Anna, Piazza Martiri della Libertà 33 - 56127 Pisa, Italy
                [44 ] ENEA, Trisaia Research Center, S.S. Ionica - Km 419.5, 75026 Rotondella (Matera), Italy
                [45 ] James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
                [46 ] Barcelona Supercomputing Center, Nexus II Building, c/ Jordi Girona, 29, 08034 Barcelona, Spain
                [47 ] ICREA, Pg Lluís Companys, 23, 08010, Barcelona, Spain
                [48 ] Keygene N.V., Agro Business Park 90, 6708 PW Wageningen, The Netherlands
                [49 ] Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, 305-806, Republic of Korea
                [50 ] Life Technologies, 500 Cummings Center, Beverly, MA 01915, U.S.A
                [51 ] Life Technologies, 25 avenue de la Baltique, BP 96, 91943 Courtaboeuf Cedex 3, France
                [52 ] Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, 50829 Cologne, Germany
                [53 ] School of Agriculture, Meiji University, 1-1-1 Higashi-Mita, Tama-ku, Kawasaki-shi, Kanagawa 214-8571, Japan
                [54 ] Department of Plant Science and Plant Pathology, Montana State University, Bozeman, MT 59717, USA
                [55 ] NARO Institute of Vegetable and Tea Science, 360 Kusawa, Ano, Tsu, Mie 514-2392, Japan
                [56 ] National Institute of Plant Genome Research, New Delhi, 110 067, India
                [57 ] Plant Research International, Business Unit Bioscience, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
                [58 ] Institute of Plant Genetic Engineering, Qingdao Agricultural University, Qingdao 266109, China
                [59 ] Roche Applied Science, D-82377 Penzberg, Germany
                [60 ] Seoul National University, Department of Plant Science and Plant Genomics and Breeding Institute, Seoul, 151-921, Republic of Korea
                [61 ] Seoul National University, Department of Agricultural Biotechnology, Seoul, 151-921, Republic of Korea
                [62 ] Seoul National University, Crop Functional Genomics Center, College of Agriculture and Life Sciences, Seoul, 151-921, Republic of Korea
                [63 ] High-tech Research center, Shandong Academy of Agricultural Sciences, Jinan 250000, China
                [64 ] Institute of Vegetables, Shandong Academy of Agricultural Sciences, Jinan, Shandong, 250100, China
                [65 ] School of life sciences, Sichuan University, Chengdu, Sichuan, 610064, China
                [66 ] Sistemas Genomicos, Parque Tecnológico de Valencia, Ronda G. Marconi, 6,46980 Paterna (Valencia), Spain
                [67 ] College of Horticulture, South China Agricultural University, 510642 Guangzhou, China.
                [68 ] Syngenta Biotechnology, Inc. 3054 East Cornwallis Rd, Research Triangle Park, NC 27709 Durham, USA
                [69 ] Norwich Research Park, Norwich NR4 7UH, UK
                [70 ] Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom
                [71 ] Robert W. Holley Center and Boyce Thompson Institute for Plant Research:; United States Department of Agriculture - Agricultural Research Service, Robert W. Holley Center, Tower Road, Cornell University campus, Ithaca NY 14853, USA
                [72 ] Universidad de Malaga-Consejo Superior de Investigaciones Cientificas:; Instituto de Hortofruticultura Subtropical y Mediterranea. Departamento de Biologia Molecular y Bioquimica, 29071 Málaga, Spain
                [73 ] Centre de Regulacio Genomica, Universitat Pompeu Fabra, Dr Aiguader, 88, E-08003 Barcelona, Spain
                [74 ] Arizona Genomics Institute, BIO-5 Institute for Collaborative Research, School of Plant Sciences, Thomas W. Keating Building, 1657 E. Helen Street, Tucson AZ 85721, USA
                [75 ] Crop Bioinformatics, Institute of Crop Science and Resource Conservation, University of Bonn, 53115 Bonn, Germany
                [76 ] Department of Plant & Soil Sciences, and Delaware Biotechnology Institute, University of Delaware, Newark, Delaware 19711, USA
                [77 ] Interdisciplinary Centre for Plant Genomics and Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi, 110 021, India
                [78 ] University of East Anglia, School of Biological Sciences:; University of East Anglia, BIO, Norwich NR4 7TJ, UK
                [79 ] University of East Anglia, School of Computing Sciences:; University of East Anglia, CMP, Norwich NR4 7TJ, UK
                [80 ] Department of Biology and the UF Genetics Institute, Cancer & Genetics Research Complex 2033 Mowry Road, PO Box 103610, Gainesville FL, USA
                [81 ] Plant Genome Mapping Laboratory, 111 Riverbend Road, University of Georgia, Athens, GA 30602, USA
                [82 ] Center for Genomics and Computational Biology, School of Life Sciences, and School of Sciences, Hebei United University, Tangshan, Hebei 063000, China
                [83 ] J. Craig Venter Institute, 9704 Medical Center Drive, Rockville, MD 20850, USA
                [84 ] University of Naples “Federico II” Department of Soil, Plant, Environmental and Animal Production Sciences, Via Universita’, 100, 80055 Portici (Naples), Italy
                [85 ] Division of Plant and Crop Sciences, University of Nottingham, Sutton Bonington, Loughborough LE12 5RD, UK
                [86 ] Department of Chemistry and Biochemistry, Stephenson Research and Technology Center, University of Oklahoma, Norman, OK 73019, USA
                [87 ] CRIBI, University of Padua, via Ugo Bassi 58/B, 35131 Padova, Italy
                [88 ] Department of Microbiology, Immunology and Biochemistry, University of Tennessee Health Science Center, Memphis, USA
                [89 ] Department of Agriculture and Environmental Sciences, University of Udine, via delle Scienze 208, 33100, Udine, Italy
                [90 ] Wageningen University, Laboratory of Genetics, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
                [91 ] Wageningen University, Laboratory of Plant Breeding, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
                [92 ] Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
                [93 ] Wellcome Trust Sanger Institute Hinxton, Cambridge CB10 1SA, UK
                [94 ] Ylichron SrL, Casaccia Research Center, Via Anguillarese 301, 00123 Roma, Italy
                Author notes
                Correspondence should be addressed to: Dani Zamir ( zamir@ 123456agri.huji.ac.il ) and Giovanni Giuliano ( giovanni.giuliano@ 123456enea.it ).
                Article
                UKMS47545
                10.1038/nature11119
                3378239
                22660326

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                Funding
                Funded by: Biotechnology and Biological Sciences Research Council :
                Award ID: BB/G006199/1 || BB_
                Funded by: Biotechnology and Biological Sciences Research Council :
                Award ID: BB/C509731/1 || BB_
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