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The Robert H. Smith Institute of
Plant Sciences and Genetics
in Agriculture
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Publications

2016
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.
Alseekh, S. ; Tohge, T. ; Wendenberg, R. ; Scossa, F. ; Omranian, N. ; Li, J. ; Kleessen, S. ; Giavalisco, P. ; Pleban, T. ; Mueller-Roeber, B. ; et al. Identification And Mode Of Inheritance Of Quantitative Trait Loci For Secondary Metabolite Abundance In Tomato. Plant Cell 2015, 27, 485-512. Publisher's VersionAbstract
A large-scale metabolic quantitative trait loci (mQTL) analysis was performed on the well-characterized Solanum pennellii introgression lines to investigate the genomic regions associated with secondary metabolism in tomato fruit pericarp. In total, 679 mQTLs were detected across the 76 introgression lines. Heritability analyses revealed that mQTLs of secondary metabolism were less affected by environment than mQTLs of primary metabolism. Network analysis allowed us to assess the interconnectivity of primary and secondary metabolism as well as to compare and contrast their respective associations with morphological traits. Additionally, we applied a recently established real-time quantitative PCR platform to gain insight into transcriptional control mechanisms of a subset of the mQTLs, including those for hydroxycinnamates, acyl-sugar, naringenin chalcone, and a range of glycoalkaloids. Intriguingly, many of these compounds displayed a dominant-negative mode of inheritance, which is contrary to the conventional wisdom that secondary metabolite contents decreased on domestication. We additionally performed an exemplary evaluation of two candidate genes for glycolalkaloid mQTLs via the use of virus-induced gene silencing. The combined data of this study were compared with previous results on primary metabolism obtained from the same material and to other studies of natural variance of secondary metabolism. © 2015 American Society of Plant Biologists. All rights reserved.
Foucher, F. ; Hibrand-Saint Oyant, L. ; Hamama, L. ; Sakr, S. ; Baudino, S. ; Caissard, J. P. ; Smulder, J. M. S. ; Debener, T. ; De Riek, J. ; Torres, A. ; et al. Towards The Rose Genome Sequence And Its Use In Research And Breeding. Acta Horticulturae 2015, 1064, 167-175. Publisher's VersionAbstract
Rose is one of the most economically important ornamental crops worldwide. Rosa sp. can become a model for woody ornamentals. Its genome size is relatively small (560 Mb), its genetic history with ploïdy events is well documented, and rose has a short life for a woody plant. Furthermore, different tools are available, including transcriptomic tools, genetic maps and genetic transformation protocols. Rose represents an original model for studying some ornamental traits that cannot be addressed in other model plant species such as Arabidopsis. Some of these traits, such recurrent blooming, flower morphogenesis or scent production and emission, are of economic interest. Different groups involved in rose genetics and genomics gathered to form the 'Rose Genome Sequence Initiative'. Our objective is to obtain a high quality rose genome sequence of the diploid R. chinensis 'Old Blush'. One important issue is the high level of heterozygosity of roses. To tackle this issue, different strategies are proposed: production of a haploid and development a high density genetic map to anchor the genome. This genetic map will be developed from a cross between 'Old Blush' and R. wichurana. The genotype R. chinensis 'Old Blush' will be sequenced using NGS technologies. The data will be assembled and arranged using the high-density map. In order to increase ESTs and to facilitate genome annotation, we have recently produced ESTs from various tissues of 'Old Blush' under different conditions. Digital expression (RNA Seq) was obtained from the different tissues and data are available on the following web site (https://iant.toulouse.inra.fr/plants/rosa/FATAL/). The rose genome sequence will be a great step to help identifying the molecular basis of ornamental traits and also to study genetic diversity and genome evolution in the genus Rosa and in the Rosaceae family. © 2015, International Society for Horticultural Science. All rights reserved.
Gur, A. ; Zamir, D. . Mendelizing All Components Of A Pyramid Of Three Yield Qtl In Tomato. Front Plant Sci 2015, 6, 1096.Abstract
Molecular markers allowed breeders to mendelize quantitative trait loci (QTL) providing another demonstration that quantitative traits are governed by the same principles as single qualitative genes. This research extends the QTL analysis to two and three QTL and tests our ability to mendelize an oligogenic trait. In tomato, agricultural yield is determined by the weight of the fruits harvested per unit area and the total soluble solids (% Brix)-sugars and acids. The current study explores the segregation of multiple independent yield-related QTL that were identified and mapped using introgression lines (IL) of Solanum pennellii in cultivated processing tomato (S. lycopersicum). We screened 45 different double and triple IL-QTL combinations for agricultural yield, to identify QTL pyramids that behaved in an additive manner and were suitable substrate for mendelizing an oligogenic trait. A pyramid of three independent QTL that significantly improved Brix(∗)Yield (BXY - the soluble solids output per unit area) compared to M82 was selected. In the progenies of the tri-hybrid we bred using markers a nearly isogenic 'immortalized F2.' While the common mode of QTL-QTL interactions across the 45 IL-QTLs combinations was less than additive, the three QTLs in the selected triple-stack performed in an additive manner which made it an exceptional material for breeding. This study demonstrates that using the phenotypic effect of all 27 possible QTL-alleles combinations it is possible to make reliable predictions about the genotypes that will maximize the yield.
Ning, J. ; Moghe, G. D. ; Leong, B. ; Kim, J. ; Ofner, I. ; Wang, Z. ; Adams, C. ; Jones, D. A. ; Zamir, D. ; Last, R. L. . A Feedback-Insensitive Isopropylmalate Synthase Affects Acylsugar Composition In Cultivated And Wild Tomato. Plant Physiol 2015, 169, 1821-35.Abstract
Acylsugars are insecticidal specialized metabolites produced in the glandular trichomes of plants in the Solanaceae family. In the tomato clade of the Solanum genus, acylsugars consist of aliphatic acids of different chain lengths esterified to sucrose, or less frequently to glucose. Through liquid chromatography-mass spectrometry screening of introgression lines, we previously identified a region of chromosome 8 in the Solanum pennellii LA0716 genome (IL8-1/8-1-1) that causes the cultivated tomato Solanum lycopersicum to shift from producing acylsucroses with abundant 3-methylbutanoic acid acyl chains derived from leucine metabolism to 2-methylpropanoic acid acyl chains derived from valine metabolism. We describe multiple lines of evidence implicating a trichome-expressed gene from this region as playing a role in this shift. S. lycopersicum M82 SlIPMS3 (Solyc08g014230) encodes a functional end product inhibition-insensitive version of the committing enzyme of leucine biosynthesis, isopropylmalate synthase, missing the carboxyl-terminal 160 amino acids. In contrast, the S. pennellii LA0716 IPMS3 allele found in IL8-1/8-1-1 encodes a nonfunctional truncated IPMS protein. M82 transformed with an SlIPMS3 RNA interference construct exhibited an acylsugar profile similar to that of IL8-1-1, whereas the expression of SlIPMS3 in IL8-1-1 partially restored the M82 acylsugar phenotype. These IPMS3 alleles are polymorphic in 14 S. pennellii accessions spread throughout the geographical range of occurrence for this species and are associated with acylsugars containing varying amounts of 2-methylpropanoic acid and 3-methylbutanoic acid acyl chains.
2014
Bolger, A. ; Scossa, F. ; Bolger, M. E. ; Lanz, C. ; Maumus, F. ; Tohge, T. ; Quesneville, H. ; Alseekh, S. ; Sørensen, I. ; Lichtenstein, G. ; et al. The Genome Of The Stress-Tolerant Wild Tomato Species Solanum Pennellii. Nature Genetics 2014, 46, 1034-1038. Publisher's VersionAbstract
Solanum pennellii is a wild tomato species endemic to Andean regions in South America, where it has evolved to thrive in arid habitats. Because of its extreme stress tolerance and unusual morphology, it is an important donor of germplasm for the cultivated tomato Solanum lycopersicum. Introgression lines (ILs) in which large genomic regions of S. lycopersicum are replaced with the corresponding segments from S. pennellii can show remarkably superior agronomic performance. Here we describe a high-quality genome assembly of the parents of the IL population. By anchoring the S. pennellii genome to the genetic map, we define candidate genes for stress tolerance and provide evidence that transposable elements had a role in the evolution of these traits. Our work paves a path toward further tomato improvement and for deciphering the mechanisms underlying the myriad other agronomic traits that can be improved with S. pennellii germplasm. © 2014 Nature America, Inc. All rights reserved.
Lin, T. ; Zhu, G. ; Zhang, J. ; Xu, X. ; Yu, Q. ; Zheng, Z. ; Zhang, Z. ; Lun, Y. ; Li, S. ; Wang, X. ; et al. Genomic Analyses Provide Insights Into The History Of Tomato Breeding; 2014; Vol. 46, pp. 1220-1226. Publisher's VersionAbstract
The histories of crop domestication and breeding are recorded in genomes. Although tomato is a model species for plant biology and breeding, the nature of human selection that altered its genome remains largely unknown. Here we report a comprehensive analysis of tomato evolution based on the genome sequences of 360 accessions. We provide evidence that domestication and improvement focused on two independent sets of quantitative trait loci (QTLs), resulting in modern tomato fruit a 1/4100 times larger than its ancestor. Furthermore, we discovered a major genomic signature for modern processing tomatoes, identified the causative variants that confer pink fruit color and precisely visualized the linkage drag associated with wild introgressions. This study outlines the accomplishments as well as the costs of historical selection and provides molecular insights toward further improvement. © 2014 Nature America, Inc. All rights reserved.
Park, S. J. ; Jiang, K. ; Tal, L. ; Yichie, Y. ; Gar, O. ; Zamir, D. ; Eshed, Y. ; Lippman, Z. B. . Optimization Of Crop Productivity In Tomato Using Induced Mutations In The Florigen Pathway. Nature Genetics 2014, 46, 1337-1342. Publisher's VersionAbstract
Naturally occurring genetic variation in the universal florigen flowering pathway has produced major advancements in crop domestication. However, variants that can maximize crop yields may not exist in natural populations. Here we show that tomato productivity can be fine-tuned and optimized by exploiting combinations of selected mutations in multiple florigen pathway components. By screening for chemically induced mutations that suppress the bushy, determinate growth habit of field tomatoes, we isolated a new weak allele of the florigen gene SINGLE FLOWER TRUSS (SFT) and two mutations affecting a bZIP transcription factor component of the 'florigen activation complex' (ref. 11). By combining heterozygous mutations, we pinpointed an optimal balance of flowering signals, resulting in a new partially determinate architecture that translated to maximum yields. We propose that harnessing mutations in the florigen pathway to customize plant architecture and flower production offers a broad toolkit to boost crop productivity. © 2014 Nature America, Inc. All rights reserved.
Neuman, H. ; Galpaz, N. ; Cunningham Jr., F. X. ; Zamir, D. ; Hirschberg, J. . The Tomato Mutation Nxd1 Reveals A Gene Necessary For Neoxanthin Biosynthesis And Demonstrates That Violaxanthin Is A Sufficient Precursor For Abscisic Acid Biosynthesis. Plant Journal 2014, 78, 80-93. Publisher's VersionAbstract
Carotenoid pigments are indispensable for plant life. They are synthesized within plastids where they provide essential functions in photosynthesis. Carotenoids serve as precursors for the synthesis of the strigolactone phytohormones, which are made from β-carotene, and of abscisic acid (ABA), which is produced from certain xanthophylls. Despite the significant progress that has been made in our understanding of the carotenoid biosynthesis pathway, the synthesis of the xanthophyll neoxanthin has remained unknown. We report here on the isolation of a tomato (Solanum lycopersicum) mutant, neoxanthin-deficient 1 (nxd1), which lacks neoxanthin, and on the cloning of a gene that is necessary for neoxanthin synthesis in both tomato and Arabidopsis. The locus nxd1 encodes a gene of unknown function that is conserved in all higher plants. The activity of NXD1 is essential but cannot solely support neoxanthin synthesis. Lack of neoxanthin does not significantly reduce the fitness of tomato plants in cultivated field conditions and does not impair the synthesis of ABA, suggesting that in tomato violaxanthin is a sufficient precursor for ABA production in vivo. © 2014 John Wiley & Sons Ltd.
Zamir, D. . A Wake-Up Call With Coffee. Science 2014, 345, 1124. Publisher's Version