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Publications

2020
Karniel, U. ; Koch, A. ; Zamir, D. ; Hirschberg, J. Development of zeaxanthin-rich tomato fruit through genetic manipulations of carotenoid biosynthesis. Plant Biotechnology Journal 2020, 18, 2292-2303. Publisher's VersionAbstract
Summary The oxygenated carotenoid zeaxanthin provides numerous benefits to human health due to its antioxidant properties. Especially it is linked to protecting, together with the xanthophyll lutein, the retina in the human eye by filtering harmful blue light thus delaying the progression of age-related macular degeneration (AMD), the most prevalent cause of blindness in developed countries. Despite its high nutritional value, zeaxanthin is less available than other substantial carotenoids in our diet. To solve this shortage, we chose to develop a new food source that would contain a high concentration of natural zeaxanthin. Tomato (Solanum lycopersicum L.) was selected as the target plant since it is the second largest vegetable crop grown worldwide and its fruit characteristically synthesizes and accumulates a high concentration of carotenoids. We employed two genetic approaches in order to enhance zeaxanthin biosynthesis in tomato fruit: a transgenic metabolic engineering and classical genetic breeding. A nontransgenic tomato line, named ‘Xantomato’, was generated whose fruit accumulated zeaxanthin at a concentration of 39 μg/g fresh weight (or 577 μg/g dry weight), which comprised ca. 50% of total fruit carotenoids compared to zero in the wild type. This is the highest concentration of zeaxanthin reached in a primary crop. Xantomato can potentially increase zeaxanthin availability in the human diet and serve as raw material for industrial applications.
Szymański, J. ; Bocobza, S. ; Panda, S. ; Sonawane, P. ; Cárdenas, P. D. ; Lashbrooke, J. ; Kamble, A. ; Shahaf, N. ; Meir, S. ; Bovy, A. ; et al. Analysis of wild tomato introgression lines elucidates the genetic basis of transcriptome and metabolome variation underlying fruit traits and pathogen response. 2020, 52, 1111 - 1121. Publisher's VersionAbstract
Wild tomato species represent a rich gene pool for numerous desirable traits lost during domestication. Here, we exploited an introgression population representing wild desert-adapted species and a domesticated cultivar to establish the genetic basis of gene expression and chemical variation accompanying the transfer of wild-species-associated fruit traits. Transcriptome and metabolome analysis of 580 lines coupled to pathogen sensitivity assays resulted in the identification of genomic loci associated with levels of hundreds of transcripts and metabolites. These associations occurred in hotspots representing coordinated perturbation of metabolic pathways and ripening-related processes. Here, we identify components of the Solanum alkaloid pathway, as well as genes and metabolites involved in pathogen defense and linking fungal resistance with changes in the fruit ripening regulatory network. Our results outline a framework for understanding metabolism and pathogen resistance during tomato fruit ripening and provide insights into key fruit quality traits.
Fich, E. A. ; Fisher, J. ; Zamir, D. ; Rose, J. K. C. Transpiration from Tomato Fruit Occurs Primarily via Trichome-Associated Transcuticular Polar Pores. Plant Physiology 2020, 184, 1840–1852. Publisher's VersionAbstract
Nonstomatal water loss by transpiration through the hydrophobic cuticle is ubiquitous in land plants, but the pathways along which this occurs have not been identified. Tomato (Solanum lycopersicum) provides an excellent system in which to study this phenomenon, as its fruit are astomatous and a major target for desiccation resistance to enhance shelf life. We screened a tomato core collection of 398 accessions from around the world and selected seven cultivars that collectively exhibited the lowest and highest degrees of transpirational water loss for a more detailed study. The transpirational differences between these lines reflected the permeances of their isolated cuticles, but this did not correlate with various measures of cuticle abundance or composition. Rather, we found that fruit cuticle permeance has a strong dependence on the abundance of microscopic polar pores. We further observed that these transcuticular pores are associated with trichomes and are exposed when the trichomes are dislodged, revealing a previously unreported link between fruit trichome density and transpirational water loss. During postharvest storage, limited self-sealing of the pores was detected for certain cultivars, in contrast with the stem scar, which healed relatively rapidly. The abundance of trichome-associated pores, together with their self-sealing capacity, presents a promising target for breeding or engineering efforts to reduce fruit transpirational water loss.
2019
Cárdenas, P. D. ; Sonawane, P. D. ; Heinig, U. ; Jozwiak, A. ; Panda, S. ; Abebie, B. ; Kazachkova, Y. ; Pliner, M. ; Unger, T. ; Wolf, D. ; et al. Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases. Nat Commun 2019, 10, 5169.Abstract
The genus Solanum comprises three food crops (potato, tomato, and eggplant), which are consumed on daily basis worldwide and also producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs). Hydroxylated SGAs (i.e. leptinines) serve as precursors for leptines that act as defenses against Colorado Potato Beetle (Leptinotarsa decemlineata Say), an important pest of potato worldwide. However, SGA hydroxylating enzymes remain unknown. Here, we discover that 2-OXOGLUTARATE-DEPENDENT-DIOXYGENASE (2-ODD) enzymes catalyze SGA-hydroxylation across various Solanum species. In contrast to cultivated potato, Solanum chacoense, a widespread wild potato species, has evolved a 2-ODD enzyme leading to the formation of leptinines. Furthermore, we find a related 2-ODD in tomato that catalyzes the hydroxylation of the bitter α-tomatine to hydroxytomatine, the first committed step in the chemical shift towards downstream ripening-associated non-bitter SGAs (e.g. esculeoside A). This 2-ODD enzyme prevents bitterness in ripe tomato fruit consumed today which otherwise would remain unpleasant in taste and more toxic.
Cárdenas, P. D. ; Sonawane, P. D. ; Heinig, U. ; Jozwiak, A. ; Panda, S. ; Abebie, B. ; Kazachkova, Y. ; Pliner, M. ; Unger, T. ; Wolf, D. ; et al. Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases. Nature Communications 2019, 10. Publisher's VersionAbstract
The genus Solanum comprises three food crops (potato, tomato, and eggplant), which are consumed on daily basis worldwide and also producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs). Hydroxylated SGAs (i.e. leptinines) serve as precursors for leptines that act as defenses against Colorado Potato Beetle (Leptinotarsa decemlineata Say), an important pest of potato worldwide. However, SGA hydroxylating enzymes remain unknown. Here, we discover that 2-OXOGLUTARATE-DEPENDENT-DIOXYGENASE (2-ODD) enzymes catalyze SGA-hydroxylation across various Solanum species. In contrast to cultivated potato, Solanum chacoense, a widespread wild potato species, has evolved a 2-ODD enzyme leading to the formation of leptinines. Furthermore, we find a related 2-ODD in tomato that catalyzes the hydroxylation of the bitter α-tomatine to hydroxytomatine, the first committed step in the chemical shift towards downstream ripening-associated non-bitter SGAs (e.g. esculeoside A). This 2-ODD enzyme prevents bitterness in ripe tomato fruit consumed today which otherwise would remain unpleasant in taste and more toxic. © 2019, The Author(s).
Brog, Y. M. ; Osorio, S. ; Yichie, Y. ; Alseekh, S. ; Bensal, E. ; Kochevenko, A. ; Zamir, D. ; Fernie, A. R. A Solanum neorickii introgression population providing a powerful complement to the extensively characterized Solanum pennellii population. Plant Journal 2019, 97, 391-403. Publisher's VersionAbstract
We present a complementary resource for trait fine-mapping in tomato to those based on the intra-specific cross between cultivated tomato and the wild tomato species Solanum pennellii, which have been extensively used for quantitative genetics in tomato over the last 20 years. The current population of backcross inbred lines (BILs) is composed of 107 lines derived after three backcrosses of progeny of the wild species Solanum neorickii (LA2133) and cultivated tomato (cultivar TA209) and is freely available to the scientific community. These S. neorickii BILs were genotyped using the 10K SolCAP single nucleotide polymorphism chip, and 3111 polymorphic markers were used to map recombination break points relative to the physical map of Solanum lycopersicum. The BILs harbor on average 4.3 introgressions per line, with a mean introgression length of 34.7 Mbp, allowing partitioning of the genome into 340 bins and thereby facilitating rapid trait mapping. We demonstrate the power of using this resource in comparison with archival data from the S. pennellii resources by carrying out metabolic quantitative trait locus analysis following gas chromatography–mass spectrometry on fruits harvested from the S. neorickii BILs. The metabolic candidate genes phenylalanine ammonia-lyase and cystathionine gamma-lyase were then tested and validated in F 2 populations and via agroinfiltration-based overexpression in order to exemplify the fidelity of this method in identifying the genes that drive tomato metabolic phenotypes. © 2018 The Authors. The Plant Journal © 2018 John Wiley & Sons Ltd and Society for Experimental Biology.
2018
Garbowicz, K. ; Liu, Z. ; Alseekh, S. ; Tieman, D. ; Taylor, M. ; Kuhalskaya, A. ; Ofner, I. ; Zamir, D. ; Klee, H. J. ; Fernie, A. R. ; et al. Quantitative Trait Loci Analysis Identifies a Prominent Gene Involved in the Production of Fatty Acid-Derived Flavor Volatiles in Tomato. Molecular Plant 2018, 11, 1147-1165. Publisher's VersionAbstract
To gain insight into the genetic regulation of lipid metabolism in tomato, we conducted metabolic trait loci (mQTL) analysis following the lipidomic profiling of fruit pericarp and leaf tissue of the Solanum pennellii introgression lines (IL). To enhance mapping resolution for selected fruit-specific mQTL, we profiled the lipids in a subset of independently derived S. pennellii backcross inbred lines, as well as in a near-isogenic sub-IL population. We identified a putative lecithin:cholesterol acyltransferase that controls the levels of several lipids, and two members of the class III lipase family, LIP1 and LIP2, that were associated with decreased levels of diacylglycerols (DAGs) and triacylglycerols (TAGs). Lipases of this class cleave fatty acids from the glycerol backbone of acylglycerols. The released fatty acids serve as precursors of flavor volatiles. We show that LIP1 expression correlates with fatty acid-derived volatile levels. We further confirm the function of LIP1 in TAG and DAG breakdown and volatile synthesis using transgenic plants. Taken together, our study extensively characterized the genetic architecture of lipophilic compounds in tomato and demonstrated at molecular level that release of free fatty acids from the glycerol backbone can have a major impact on downstream volatile synthesis. In this work, we conducted large-scale lipid profiling of fruit pericarp and leaf materials of a population of S. pennellii introgression line to gain insight into the genetic regulation of lipid metabolism in tomato. By combination of QTL mapping, metabolic and transcriptomic data, we identified and cloned novel lipid–genes that have a major effect on production of multiple fatty acid-derived flavor volatiles. These metabolites are positively correlated with consumer liking and are crucial for key agronomical traits in tomato. © 2018 The Author
2017
Soyk, S. ; Lemmon, Z. H. ; Oved, M. ; Fisher, J. ; Liberatore, K. L. ; Park, S. J. ; Goren, A. ; Jiang, K. ; Ramos, A. ; van der Knaap, E. ; et al. Bypassing Negative Epistasis on Yield in Tomato Imposed by a Domestication Gene. Cell 2017, 169, 1142-1155.e12. Publisher's VersionAbstract
Selection for inflorescence architecture with improved flower production and yield is common to many domesticated crops. However, tomato inflorescences resemble wild ancestors, and breeders avoided excessive branching because of low fertility. We found branched variants carry mutations in two related transcription factors that were selected independently. One founder mutation enlarged the leaf-like organs on fruits and was selected as fruit size increased during domestication. The other mutation eliminated the flower abscission zone, providing “jointless” fruit stems that reduced fruit dropping and facilitated mechanical harvesting. Stacking both beneficial traits caused undesirable branching and sterility due to epistasis, which breeders overcame with suppressors. However, this suppression restricted the opportunity for productivity gains from weak branching. Exploiting natural and engineered alleles for multiple family members, we achieved a continuum of inflorescence complexity that allowed breeding of higher-yielding hybrids. Characterizing and neutralizing similar cases of negative epistasis could improve productivity in many agricultural organisms. Video Abstract © 2017 Elsevier Inc.
Alseekh, S. ; Tong, H. ; Scossa, F. ; Brotman, Y. ; Vigroux, F. ; Tohge, T. ; Ofner, I. ; Zamir, D. ; Nikoloski, Z. ; Fernie, A. R. Canalization of tomato fruit metabolism. Plant Cell 2017, 29, 2753-2765. Publisher's VersionAbstract
To explore the genetic robustness (canalization) of metabolism, we examined the levels of fruit metabolites in multiple harvests of a tomato introgression line (IL) population. The IL partitions the whole genome of the wild species Solanum pennellii in the background of the cultivated tomato (Solanum lycopersicum). We identified several metabolite quantitative trait loci that reduce variability for both primary and secondary metabolites, which we named canalization metabolite quantitative trait loci (cmQTL). We validated nine cmQTL using an independent population of backcross inbred lines, derived from the same parents, which allows increased resolution in mapping the QTL previously identified in the ILs. These cmQTL showed little overlap with QTL for the metabolite levels themselves. Moreover, the intervals they mapped to harbored few metabolism-associated genes, suggesting that the canalization of metabolism is largely controlled by regulatory genes. © American Society of Plant Biologists.
Tieman, D. ; Zhu, G. ; Resende, M.F., J. ; Lin, T. ; Nguyen, C. ; Bies, D. ; Rambla, J. L. ; Beltran, K. S. ; Taylor, M. ; Zhang, B. ; et al. A chemical genetic roadmap to improved tomato flavor. Science (New York, N.Y.) 2017, 355, 391-394. Publisher's VersionAbstract
Modern commercial tomato varieties are substantially less flavorful than heirloom varieties. To understand and ultimately correct this deficiency, we quantified flavor-associated chemicals in 398 modern, heirloom, and wild accessions. A subset of these accessions was evaluated in consumer panels, identifying the chemicals that made the most important contributions to flavor and consumer liking. We found that modern commercial varieties contain significantly lower amounts of many of these important flavor chemicals than older varieties. Whole-genome sequencing and a genome-wide association study permitted identification of genetic loci that affect most of the target flavor chemicals, including sugars, acids, and volatiles. Together, these results provide an understanding of the flavor deficiencies in modern commercial varieties and the information necessary for the recovery of good flavor through molecular breeding. Copyright © 2017, American Association for the Advancement of Science.
Schmidt, M. H. - W. ; Vogel, A. ; Denton, A. K. ; Istace, B. ; Wormit, A. ; van de Geest, H. ; Bolger, M. E. ; Alseekh, S. ; Maß, J. ; Pfaff, C. ; et al. De novo assembly of a new Solanum pennellii accession using nanopore sequencing. Plant Cell 2017, 29, 2336-2348. Publisher's VersionAbstract
Updates in nanopore technology have made it possible to obtain gigabases of sequence data. Prior to this, nanopore sequencing technology was mainly used to analyze microbial samples. Here, we describe the generation of a comprehensive nanopore sequencing data set with a median read length of 11,979 bp for a self-compatible accession of the wild tomato species Solanum pennellii. We describe the assembly of its genome to a contig N50 of 2.5 MB. The assembly pipeline comprised initial read correction with Canu and assembly with SMARTdenovo. The resulting raw nanopore-based de novo genome is structurally highly similar to that of the reference S. pennellii LA716 accession but has a high error rate and was rich in homopolymer deletions. After polishing the assembly with Illumina reads, we obtained an error rate of <0.02% when assessed versus the same Illumina data. We obtained a gene completeness of 96.53%, slightly surpassing that of the reference S. pennellii. Taken together, our data indicate that such long read sequencing data can be used to affordably sequence and assemble gigabase-sized plant genomes. © 2017 The author(s).
Fisher, J. ; Bensal, E. ; Zamir, D. Bimodality of stable and plastic traits in plants. Theor Appl Genet 2017, 130, 1915-1926.Abstract
KEY MESSAGE: We discovered an unexpected mode of bimodal distribution of stable and plastic traits, which was consistent for homologous traits of 32 varieties of seven species both in well-irrigated fields and dry conditions. We challenged archived genetic mapping data for 36 fruit, seed, flower and yield traits in tomato and found an unexpected bimodal distribution in one measure of trait variability, the mean coefficient of variation, with some traits being consistently more variable than others. To determine the degree of conservation of this distribution among higher plants, we compared 18 homologous phenotypes, including yield and seed production, across different crop species grown in a common 'crop garden' experiment. The set included 32 varieties of tomato, eggplant, pepper, melon, watermelon, sunflower and maize. Estimates of canalization were obtained using a 'canalization replication' experimental design that generated multiple estimates of the coefficient of variation of traits, as well as their reaction norms in optimal and water-stressed field plots. A common pattern of bimodal distribution of stable and plastic traits was observed for all the varieties and for a wild weed (Solanum nigrum). We propose that canalization profiles of traits in a variety of taxa were ancestrally selected to maximize adaptation and reproductive success.
2016
Fan, P. ; Miller, A. M. ; Schilmiller, A. L. ; Liu, X. ; Ofner, I. ; Jones, A. D. ; Zamir, D. ; Last, R. L. In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network. Proceedings of the National Academy of Sciences of the United States of America 2016, 113, E239-E248. Publisher's VersionAbstract
Plant glandular secreting trichomes are epidermal protuberances that produce structurally diverse specialized metabolites, including medically important compounds. Trichomes of many plants in the nightshade family (Solanaceae) produce O-acylsugars, and in cultivated and wild tomatoes these are mixtures of aliphatic esters of sucrose and glucose of varying structures and quantities documented to contribute to insect defense. We characterized the first two enzymes of acylsucrose biosynthesis in the cultivated tomato Solanum lycopersicum. These are type I/IV trichome-expressed BAHD acyltransferases encoded by Solyc12g006330-or S. lycopersicum acylsucrose acyltransferase 1 (Sl-ASAT1)-and Solyc04g012020 (Sl-ASAT2). These enzymes were used.in concert with two previously identified BAHD acyltransferases. to reconstruct the entire cultivated tomato acylsucrose biosynthetic pathway in vitro using sucrose and acyl-CoA substrates. Comparative genomics and biochemical analysis of ASAT enzymes were combined with in vitro mutagenesis to identify amino acids that influence CoA ester substrate specificity and contribute to differences in types of acylsucroses that accumulate in cultivated andwild tomato species. This work demonstrates the feasibility of the metabolic engineering of these insecticidal metabolites in plants and microbes.
Fulop, D. ; Ranjan, A. ; Ofner, I. ; Covington, M. F. ; Chitwood, D. H. ; West, D. ; Ichihashi, Y. ; Headland, L. ; Zamir, D. ; Maloof, J. N. ; et al. A new advanced backcross tomato population enables high resolution leaf QTL mapping and gene identification. G3: Genes, Genomes, Genetics 2016, 6 3169-3184. Publisher's VersionAbstract
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 BC2 and BC3 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. © 2016 Fulop et al.
Zamir, D. Farewell to the Lose–Lose Reality of Policing Plant Imports. PLoS Biology 2016, 14. Publisher's VersionAbstract
In an age of free international shipments of mail-ordered seeds and plants, more policing will not stop the global migration of hitchhiking pests. The solution is in a preemptive response based on an internationally coordinated genomic deployment of global biodiversity in the largest breeding project since the “Garden of Eden.” This plan will enrich the narrow genetic basis of annual and perennial plants with adaptations to changing environments and resistances to the pests of the future. © 2016 Dani Zamir.
Pankratov, I. ; McQuinn, R. ; Schwartz, J. ; Bar, E. ; Fei, Z. ; Lewinsohn, E. ; Zamir, D. ; Giovannoni, J. J. ; Hirschberg, J. Fruit carotenoid-deficient mutants in tomato reveal a function of the plastidial isopentenyl diphosphate isomerase (IDI1) in carotenoid biosynthesis. Plant Journal 2016, 88, 82-94. Publisher's VersionAbstract
Isoprenoids consist of a large class of compounds that are present in all living organisms. They are derived from the 5C building blocks isopentenyl diphosphate (IDP) and its isomer dimethylallyl diphosphate (DMADP). In plants, IDP is synthesized in the cytoplasm from mevalonic acid via the MVA pathway, and in plastids from 2-C-methyl-d-erythritol-4-phosphate through the MEP pathway. The enzyme IDP isomerase (IDI) catalyzes the interconversion between IDP and DMADP. Most plants contain two IDI enzymes, the functions of which are characteristically compartmentalized in the cells. Carotenoids are isoprenoids that play essential roles in photosynthesis and provide colors to flowers and fruits. They are synthesized in the plastids via the MEP pathway. Fruits of Solanum lycopersicum (tomato) accumulate high levels of the red carotene lycopene. We have identified mutations in tomato that reduce overall carotenoid accumulation in fruits. Four alleles of a locus named FRUIT CAROTENOID DEFICIENT 1 (fcd1) were characterized. Map-based cloning of fcd1 indicated that this gene encodes the plastidial enzyme IDI1. Lack of IDI1 reduced the concentration of carotenoids in fruits, flowers and cotyledons, but not in mature leaves. These results indicate that the plastidial IDI plays an important function in carotenoid biosynthesis, thus highlighting its role in optimizing the ratio between IDP and DMADP as precursors for different downstream isoprenoid pathways. © 2016 The Authors The Plant Journal © 2016 John Wiley & Sons Ltd
Knapp, S. ; Zamir, D. Genomics: The language of flowers. Nature 2016, 534, 328-329. Publisher's Version
Ofner, I. ; Lashbrooke, J. ; Pleban, T. ; Aharoni, A. ; Zamir, D. Solanum pennellii backcross inbred lines (BILs) link small genomic bins with tomato traits. Plant J 2016, 87, 151-60.Abstract
We present a resource for fine mapping of traits derived from the wild tomato species Solanum pennellii (LA0716). The population of backcross inbred lines (BILs) is composed of 446 lines derived after a few generations of backcrosses of the wild species with cultivated tomato (cultivar M82; LA3475), followed by more than seven generations of self-pollination. The BILs were genotyped using the 10K SOL-CAP single nucleotide polymorphism (SNP) -Chip, and 3700 polymorphic markers were used to map recombination break points relative to the physical map of Solanum lycopersicum. The BILs carry, on average, 2.7 introgressions per line, with a mean introgression length of 11.7 Mbp. Whereas the classic 76 introgression lines (ILs) partitioned the genome into 106 mapping bins, the BILs generated 633 bins, thereby enhancing the mapping resolution of traits derived from the wild species. We demonstrate the power of the BILs for rapid fine mapping of simple and complex traits derived from the wild tomato species.
2015
Toubiana, D. ; Batushansky, A. ; Tzfadia, O. ; Scossa, F. ; Khan, A. ; Barak, S. ; Zamir, D. ; Fernie, A. R. ; Nikoloski, Z. ; Fait, A. Combined correlation-based network and mQTL analyses efficiently identified loci for branched-chain amino acid, serine to threonine, and proline metabolism in tomato seeds. Plant Journal 2015, 81, 121-133. Publisher's VersionAbstract
Correlation-based network analysis (CNA) of the metabolic profiles of seeds of a tomato introgression line mapping population revealed a clique of proteinogenic amino acids: Gly, Ile, Pro, Ser, Thr, and Val. Correlations between profiles of these amino acids exhibited a statistically significant average correlation coefficient of 0.84 as compared with an average correlation coefficient of 0.39 over the 16 119 other metabolite cliques containing six metabolites. In silico removal of cliques was used to quantify their importance in determining seminal network properties, highlighting the strong effects of the amino acid clique. Quantitative trait locus analysis revealed co-localization for the six amino acids on chromosome 2, 4 and 10. Sequence analysis identified a unique set of 10 genes on chromosome 2 only, which were associated with amino acid metabolism and specifically the metabolism of Ser-Gly and their conversion into branched-chain amino acids. Metabolite profiling of a set of sublines, with introgressions on chromosome 2, identified a significant change in the abundance of the six amino acids in comparison with M82. Expression analysis of candidate genes affecting Ser metabolism matched the observation from the metabolite data, suggesting a coordinated behavior of the level of these amino acids at the genetic level. Analysis of transcription factor binding sites in the promoter regions of the identified genes suggested combinatorial response to light and the circadian clock. Significance Statement In the current study we have effectively identified loci for branched chain amino acid, serene, glycine, threonine and proline metabolism for seeds of a tomato Introgression Line mapping population. We did so by applying a combined correlation based network approach with quantitative trait locus mapping. © 2014 The Authors The Plant Journal © 2014 John Wiley & Sons Ltd.
Müller, N. A. ; Wijnen, C. L. ; Srinivasan, A. ; Ryngajllo, M. ; Ofner, I. ; Lin, T. ; Ranjan, A. ; West, D. ; Maloof, J. N. ; Sinha, N. R. ; et al. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nature Genetics 2015, 48, 89-93. Publisher's VersionAbstract
The circadian clock is a critical regulator of plant physiology and development, controlling key agricultural traits in crop plants. In addition, natural variation in circadian rhythms is important for local adaptation. However, quantitative modulation of circadian rhythms due to artificial selection has not yet been reported. Here we show that the circadian clock of cultivated tomato (Solanum lycopersicum) has slowed during domestication. Allelic variation of the tomato homolog of the Arabidopsis gene EID1 is responsible for a phase delay. Notably, the genomic region harboring EID1 shows signatures of a selective sweep. We find that the EID1 allele in cultivated tomatoes enhances plant performance specifically under long day photoperiods, suggesting that humans selected slower circadian rhythms to adapt the cultivated species to the long summer days it encountered as it was moved away from the equator. © 2016 Nature America, Inc.