Nunes-Nesi, A.; Alseekh, S.; de Oliveira Silva, F.M.; Omranian, N.; Lichtenstein, G.; Mirnezhad, M.; González, R.R.R.; Garcia, J.S.; Conte, M.; Leiss, K.A.; Klinkhamer, P.G.L.; Nikoloski, Z.; Carrari, F.; Fernie, A.R. "Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds" (2019) Metabolomics. 15(4)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Introduction: To date, most studies of natural variation and metabolite quantitative trait loci (mQTL) in tomato have focused on fruit metabolism, leaving aside the identification of genomic regions involved in the regulation of leaf metabolism. Objective: This study was conducted to identify leaf mQTL in tomato and to assess the association of leaf metabolites and physiological traits with the metabolite levels from other tissues. Methods: The analysis of components of leaf metabolism was performed by phenotypying 76 tomato ILs with chromosome segments of the wild species Solanum pennellii in the genetic background of a cultivated tomato (S. lycopersicum) variety M82. The plants were cultivated in two different environments in independent years and samples were harvested from mature leaves of non-flowering plants at the middle of the light period. The non-targeted metabolite profiling was obtained by gas chromatography time-of-flight mass spectrometry (GC-TOF-MS). With the data set obtained in this study and already published metabolomics data from seed and fruit, we performed QTL mapping, heritability and correlation analyses. Results: Changes in metabolite contents were evident in the ILs that are potentially important with respect to stress responses and plant physiology. By analyzing the obtained data, we identified 42 positive and 76 negative mQTL involved in carbon and nitrogen metabolism. Conclusions: Overall, these findings allowed the identification of S. lycopersicum genome regions involved in the regulation of leaf primary carbon and nitrogen metabolism, as well as the association of leaf metabolites with metabolites from seeds and fruits. © 2019, The Author(s).


Documento: Artículo
Título:Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds
Autor:Nunes-Nesi, A.; Alseekh, S.; de Oliveira Silva, F.M.; Omranian, N.; Lichtenstein, G.; Mirnezhad, M.; González, R.R.R.; Garcia, J.S.; Conte, M.; Leiss, K.A.; Klinkhamer, P.G.L.; Nikoloski, Z.; Carrari, F.; Fernie, A.R.
Filiación:Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais 36570-900, Brazil
Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, Potsdam, Golm, OT 14476, Germany
Center of Plant System Biology and Biotechnology (CPSBB), Plovdiv, Bulgaria
Instituto de Biotecnología, Instituto Nacional de Tecnología Agropecuaría, Consejo Nacional de Investigaciones Científicas y Técnicas, Castelar, B1712WAA, Argentina
Plant Ecology, Institute of Biology, Leiden University, Sylviusweg 72, Leiden, 2333 BE, Netherlands
Bioinformatics Group, Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany
Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-UBA-CONICET), Universidad de Buenos Aires, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina
Facultad de Agronomía, Cátedra de Genética, Universidad de Buenos Aires, Buenos Aires, Argentina
Business Unit Horticulture, Wageningen University & Research, Postbus 20, Bleiswijk, 2665 ZG, Netherlands
Palabras clave:Leaf metabolism; Metabolite network; Metabolite QTL; Tomato; alanine; aspartic acid; fructose; glucose; glutamic acid; glyceric acid; glycine; isoleucine; leucine; nitrogen; proline; psicose; serine; sucrose; tyrosine; allele; amino acid analysis; Article; biotic stress; electron transport; gas chromatography; gene expression; gene location; genetic background; genetic variation; genotype; harvest index; mass fragmentography; metabolite; metabolomics; nonhuman; phenotype; photosynthesis; plant gene; plant growth; plant leaf; quantitative trait locus; time of flight mass spectrometry; tomato
Título revista:Metabolomics
Título revista abreviado:Metabolomics
CAS:alanine, 56-41-7, 6898-94-8; aspartic acid, 56-84-8, 6899-03-2; fructose, 30237-26-4, 57-48-7, 7660-25-5, 77907-44-9; glucose, 50-99-7, 84778-64-3; glutamic acid, 11070-68-1, 138-15-8, 56-86-0, 6899-05-4; glyceric acid, 473-81-4; glycine, 56-40-6, 6000-43-7, 6000-44-8; isoleucine, 7004-09-3, 73-32-5; leucine, 61-90-5, 7005-03-0; nitrogen, 7727-37-9; proline, 147-85-3, 7005-20-1; psicose, 23140-52-5; serine, 56-45-1, 6898-95-9; sucrose, 122880-25-5, 57-50-1; tyrosine, 16870-43-2, 55520-40-6, 60-18-4


  • Alseekh, S., Ofner, I., Pleban, T., Tripodi, P., Di Dato, F., Cammareri, M., Resolution by recombination: breaking up Solanum pennellii introgressions (2013) Trends in Plant Science, 18 (10), pp. 536-538. , COI: 1:CAS:528:DC%2BC3sXhsVWisL7E, PID: 24029406
  • Alseekh, S., Tohge, T., Wendenberg, R., Scossa, F., Omranian, N., Li, J., Identification and mode of inheritance of quantitative trait loci for secondary metabolite abundance in tomato (2015) The Plant Cell, 27 (3), pp. 485-512. , COI: 1:CAS:528:DC%2BC2MXntFOms70%3D, PID: 25770107
  • Alseekh, S., Tong, H., Scossa, F., Brotman, Y., Vigroux, F., Tohge, T., Canalization of tomato fruit metabolism (2017) The Plant Cell, 29 (11), pp. 2753-2765. , COI: 1:CAS:528:DC%2BC1cXhsFelurvM, PID: 29093214
  • Araujo, W.L., Nunes-Nesi, A., Osorio, S., Usadel, B., Fuentes, D., Nagy, R., Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture (2011) The Plant Cell, 23 (2), pp. 600-627. , COI: 1:CAS:528:DC%2BC3MXkvVOrsrs%3D, PID: 21307286
  • Ballester, A.R., Tikunov, Y., Molthoff, J., Grandillo, S., Viquez-Zamora, M., de Vos, R., Identification of Loci affecting accumulation of secondary metabolites in tomato fruit of a Solanum lycopersicum x Solanum chmielewskii introgression line population (2016) Frontiers in Plant Science, 7, p. 1428. , PID: 27733856
  • Baxter, C.J., Carrari, F., Bauke, A., Overy, S., Hill, S.A., Quick, P.W., Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids (2005) Plant & Cell Physiology, 46 (3), pp. 425-437. , COI: 1:CAS:528:DC%2BD2MXjtVyisrk%3D
  • Bolger, A., Scossa, F., Bolger, M.E., Lanz, C., Maumus, F., Tohge, T., The genome of the stress-tolerant wild tomato species Solanum pennellii (2014) Nature Genetics, 46 (9), pp. 1034-1038. , COI: 1:CAS:528:DC%2BC2cXht1ait7%2FI, PID: 25064008
  • Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M.I., Nunes-Nesi, A., Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior (2006) Plant Physiology, 142 (4), pp. 1380-1396. , COI: 1:CAS:528:DC%2BD28XhtlCns7rP, PID: 17071647
  • Causse, M., Duffe, P., Gomez, M.C., Buret, M., Damidaux, R., Zamir, D., A genetic map of candidate genes and QTLs involved in tomato fruit size and composition (2004) Journal of Experimental Botany, 55 (403), pp. 1671-1685. , COI: 1:CAS:528:DC%2BD2cXntValtrY%3D, PID: 15258170
  • Chan, E.K., Rowe, H.C., Hansen, B.G., Kliebenstein, D.J., The complex genetic architecture of the metabolome (2010) PLoS Genetics, 6 (11). , PID: 21079692
  • Chitwood, D.H., Kumar, R., Headland, L.R., Ranjan, A., Covington, M.F., Ichihashi, Y., A quantitative genetic basis for leaf morphology in a set of precisely defined tomato introgression lines (2013) The Plant Cell, 25 (7), pp. 2465-2481. , COI: 1:CAS:528:DC%2BC3sXhsVKksbzJ, PID: 23872539
  • Chitwood, D.H., Maloof, J.N., Sinha, N.R., Dynamic transcriptomic profiles between tomato and a wild relative reflect distinct developmental architectures (2013) Plant Physiology, 162 (2), pp. 537-552. , COI: 1:CAS:528:DC%2BC3sXps1Oruro%3D, PID: 23585653
  • Cruz, C.D., GENES—a software package for analysis in experimental statistics and quantitative genetics (2013) Acta Scientiarum Agronomy, 35 (3), pp. 271-276
  • de Oliveira Silva, F.M., de Ávila Silva, L., Araújo, W.L., Zsögön, A., Nunes-Nesi, A., Exploiting natural variation to discover candidate genes involved in photosynthesis-related traits (2017) Methods in Molecular Biology, 1653, pp. 125-135. , PID: 28822130
  • de Oliveira Silva, F.M., Lichtenstein, G., Alseekh, S., Rosado-Souza, L., Conte, M., Suguiyama, V.F., The genetic architecture of photosynthesis and plant growth-related traits in tomato (2018) Plant, Cell & Environment, 41 (2), pp. 327-341
  • Desbrosses, G.G., Kopka, J., Udvardi, M.K., Lotus japonicus metabolic profiling. Development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions (2005) Plant Physiology, 137 (4), pp. 1302-1318. , COI: 1:CAS:528:DC%2BD2MXjslaqurg%3D, PID: 15749991
  • Dixon, R.A., Strack, D., Phytochemistry meets genome analysis, and beyond (2003) Phytochemistry, 62 (6), pp. 815-816. , COI: 1:CAS:528:DC%2BD3sXhtVelsbg%3D, PID: 12590109
  • Do, P.T., Prudent, M., Sulpice, R., Causse, M., Fernie, A.R., The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population (2010) Plant Physiology, 154 (3), pp. 1128-1142. , COI: 1:CAS:528:DC%2BC3cXhsV2ntr7N, PID: 20841452
  • Eshed, Y., Zamir, D., An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL (1995) Genetics, 141 (3), pp. 1147-1162. , COI: 1:CAS:528:DyaK28Xht1CltLw%3D, PID: 8582620
  • Fan, P., Miller, A.M., Liu, X., Jones, A.D., Last, R.L., Evolution of a flipped pathway creates metabolic innovation in tomato trichomes through BAHD enzyme promiscuity (2017) Nature Communications, 8 (1), p. 2080
  • Fanourakis, D., Giday, H., Milla, R., Pieruschka, R., Kjaer, K.H., Bolger, M., Pore size regulates operating stomatal conductance, while stomatal densities drive the partitioning of conductance between leaf sides (2015) Annals of Botany, 115 (4), pp. 555-565. , COI: 1:CAS:528:DC%2BC1cXpslahuw%3D%3D, PID: 25538116
  • Fernie, A.R., Aharoni, A., Willmitzer, L., Stitt, M., Tohge, T., Kopka, J., Recommendations for reporting metabolite data (2011) The Plant Cell, 23 (7), pp. 2477-2482. , COI: 1:CAS:528:DC%2BC3MXhtFeqs7fE, PID: 21771932
  • Fridman, E., Carrari, F., Liu, Y.S., Zamir, D., Zooming in on a quantitative trait for tomato yield using interspecific introgressions (2004) Science, 305 (5691), pp. 1786-1789. , COI: 1:CAS:528:DC%2BD2cXnsFajur8%3D, PID: 15375271
  • Gago, J., Fernie, A.R., Nikoloski, Z., Tohge, T., Martorell, S., Escalona, J.M., Integrative field scale phenotyping for investigating metabolic components of water stress within a vineyard (2017) Plant Methods, 13, p. 90. , PID: 29093742
  • Garbowicz, K., Liu, Z., Alseekh, S., Tieman, D., Taylor, M., Kuhalskaya, A., Quantitative trait loci analysis identifies a prominent gene involved in the production of fatty-acid-derived flavor volatiles in tomato (2018) Molecular Plant, 11 (9), pp. 1147-1165. , COI: 1:CAS:528:DC%2BC1cXhsVKrur%2FO, PID: 29960108
  • Hall, D., Tegstrom, C., Ingvarsson, P.K., Using association mapping to dissect the genetic basis of complex traits in plants (2010) Briefings in Functional Genomics, 9 (2), pp. 157-165. , COI: 1:CAS:528:DC%2BC3cXjvF2hu7o%3D, PID: 20053815
  • Harrigan, G.G., Stork, L.G., Riordan, S.G., Reynolds, T.L., Ridley, W.P., Impact of genetics and environment on nutritional and metabolite components of maize grain (2007) Journal of Agricultural and Food Chemistry., 55 (15), pp. 6177-6185. , COI: 1:CAS:528:DC%2BD2sXntFKqtLw%3D, PID: 17608428
  • Holtan, H.E., Hake, S., Quantitative trait locus analysis of leaf dissection in tomato using Lycopersicon pennellii segmental introgression lines (2003) Genetics, 165 (3), pp. 1541-1550. , COI: 1:CAS:528:DC%2BD2cXmsVKktw%3D%3D, PID: 14668401
  • Ingvarsson, P.K., Street, N.R., Association genetics of complex traits in plants (2011) New Phytologist, 189 (4), pp. 909-922. , PID: 21182529
  • Jansen, R.C., Tesson, B.M., Fu, J., Yang, Y., McIntyre, L.M., Defining gene and QTL networks (2009) Current Opinion in Plant Biology, 12 (2), pp. 241-246. , COI: 1:CAS:528:DC%2BD1MXjsVOgurs%3D, PID: 19196544
  • Keurentjes, J.J.B., Jingyuan, F., de Vos, C.H.R., Lommen, A., Hall, R.D., Bino, R.J., The genetics of plant metabolism (2006) Nature Genetics, 38 (7), pp. 842-849. , COI: 1:CAS:528:DC%2BD28XmtFyru78%3D, PID: 16751770
  • Kopka, J., Schauer, N., Krueger, S., Birkemeyer, C., Usadel, B., Bergmuller, E., GMD@CSBDB: the golm metabolome database (2005) Bioinformatics, 21 (8), pp. 1635-1638. , COI: 1:CAS:528:DC%2BD2MXjtlGgsrg%3D, PID: 15613389
  • Li, B., Zhang, Y., Mohammadi, S.A., Huai, D., Zhou, Y., Kliebenstein, D.J., An integrative genetic study of rice metabolism, growth and stochastic variation reveals potential C/N Partitioning Loci (2016) Scientific Reports, 6 (1), p. 30143. , COI: 1:CAS:528:DC%2BC2sXksFehsLw%3D, PID: 27440503
  • Liaw, A., Wiener, M., Classification and regression by random Forest (2002) R News, 2 (3), pp. 18-22
  • Lippman, Z.B., Semel, Y., Zamir, D., An integrated view of quantitative trait variation using tomato interspecific introgression lines (2007) Current Opinion in Genetics & Development, 17 (6), pp. 545-552. , COI: 1:CAS:528:DC%2BD2sXhsVWisb3M
  • Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., Fernie, A.R., Gas chromatography mass spectrometry-based metabolite profiling in plants (2006) Nature Protocols, 1 (1), pp. 387-396. , COI: 1:CAS:528:DC%2BD28XhtFOitbnN, PID: 17406261
  • Lisec, J., Steinfath, M., Meyer, R.C., Selbig, J., Melchinger, A.E., Willmitzer, L., Identification of heterotic metabolite QTL in Arabidopsis thaliana RIL and IL populations (2009) The Plant Journal, 59 (5), pp. 777-788. , COI: 1:CAS:528:DC%2BD1MXhtFyrtbzM, PID: 19453458
  • Liu, Y.S., Gur, A., Ronen, G., Causse, M., Damidaux, R., Buret, M., There is more to tomato fruit colour than candidate carotenoid genes (2003) Plant biotechnology journal, 1 (3), pp. 195-207. , COI: 1:CAS:528:DC%2BD3sXosFyrsrs%3D, PID: 17156032
  • Liu, Y.S., Zamir, D., Second generation L. pennellii introgression lines and the concept of bin mapping (1999) Tomato Genetics Cooperative, 49, pp. 26-30
  • López, M.G., Zanor, M.I., Pratta, G.R., Stegmayer, G., Boggio, S.B., Conte, M., Metabolic analyses of interspecific tomato recombinant inbred lines for fruit quality improvement (2015) Metabolomics, 11 (5), pp. 1416-1431
  • Luedemann, A., von Malotky, L., Erban, A., Kopka, J., TagFinder: preprocessing software for the fingerprinting and the profiling of gas chromatography-mass spectrometry based metabolome analyses (2012) Methods in Molecular Biology, 860, pp. 255-286. , COI: 1:CAS:528:DC%2BC38XhsFGlsLjL, PID: 22351182
  • Lytovchenko, A., Eickmeier, I., Pons, C., Osorio, S., Szecowka, M., Lehmberg, K., Tomato fruit photosynthesis is seemingly unimportant in primary metabolism and ripening but plays a considerable role in seed development (2011) Plant Physiology, 157 (4), pp. 1650-1663. , COI: 1:CAS:528:DC%2BC3MXhs1ekt7fL, PID: 21972266
  • Matsuba, Y., Nguyen, T.T., Wiegert, K., Falara, V., Gonzales-Vigil, E., Leong, B., Evolution of a complex locus for terpene biosynthesis in Solanum (2013) The Plant Cell, 25 (6), pp. 2022-2036. , COI: 1:CAS:528:DC%2BC3sXht1OmtrfP, PID: 23757397
  • Matsuda, F., Hirai, M.Y., Sasaki, E., Akiyama, K., Yonekura-Sakakibara, K., Provart, N.J., AtMetExpress development: a phytochemical atlas of Arabidopsis development (2010) Plant Physiology, 152 (2), pp. 566-578. , COI: 1:CAS:528:DC%2BC3cXmsFegtr4%3D, PID: 20023150
  • Matsuda, F., Yonekura-Sakakibara, K., Niida, R., Kuromori, T., Shinozaki, K., Saito, K., MS/MS spectral tag-based annotation of non-targeted profile of plant secondary metabolites (2009) The Plant Journal, 57 (3), pp. 555-577. , COI: 1:CAS:528:DC%2BD1MXit1Kiur8%3D, PID: 18939963
  • Mirnezhad, M., Romero-Gonzalez, R.R., Leiss, K.A., Choi, Y.H., Verpoorte, R., Klinkhamer, P.G., Metabolomic analysis of host plant resistance to thrips in wild and cultivated tomatoes (2010) Phytochemical Analysis, 21 (1), pp. 110-117. , COI: 1:CAS:528:DC%2BD1MXhsFGrtrnI, PID: 19866459
  • Mounet, F., Moing, A., Garcia, V., Petit, J., Maucourt, M., Deborde, C., Gene and metabolite regulatory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development (2009) Plant Physiology, 149 (3), pp. 1505-1528. , COI: 1:CAS:528:DC%2BD1MXlsFCiurk%3D, PID: 19144766
  • Ning, J., Moghe, G.D., Leong, B., Kim, J., Ofner, I., Wang, Z., A feedback-insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato (2015) Plant Physiology, 169 (3), pp. 1821-1835. , COI: 1:CAS:528:DC%2BC28Xjs1Kgu7k%3D, PID: 25986128
  • Nunes-Nesi, A., Carrari, F., Lytovchenko, A., Smith, A.M., Loureiro, M.E., Ratcliffe, R.G., Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants (2005) Plant Physiology, 137 (2), pp. 611-622. , COI: 1:CAS:528:DC%2BD2MXhs1Kqsbs%3D, PID: 15665243
  • Pnueli, L., Carmel-Goren, L., Hareven, D., Gutfinger, T., Alvarez, J., Ganal, M., The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1 (1998) Development, 125 (403), pp. 1979-1989. , COI: 1:CAS:528:DyaK1cXktFentbc%3D, PID: 9570763
  • Quadrana, L., Almeida, J., Asis, R., Duffy, T., Dominguez, P.G., Bermudez, L., Natural occurring epialleles determine vitamin E accumulation in tomato fruits (2014) Nature Communications, 5, p. 3027. , COI: 1:CAS:528:DC%2BC2cXhvF2mtbvK, PID: 24967512
  • Roessner-Tunali, U., Hegemann, B., Lytovchenko, A., Carrari, F., Bruedigam, C., Granot, D., Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development (2003) Plant Physiology, 133 (1), pp. 84-99. , COI: 1:CAS:528:DC%2BD3sXntlaitLw%3D, PID: 12970477
  • Ron, M., Dorrity, M.W., de Lucas, M., Toal, T., Hernandez, R.I., Little, S.A., Identification of novel loci regulating interspecific variation in root morphology and cellular development in tomato (2013) Plant Physiology, 162 (2), pp. 755-768. , COI: 1:CAS:528:DC%2BC3sXps1Oqsr8%3D, PID: 23575417
  • Ronen, G., Carmel-Goren, L., Zamir, D., Hirschberg, J., An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato (2000) Proceedings of the National Academy of Sciences of the United States of America, 97 (20), pp. 11102-11107. , COI: 1:CAS:528:DC%2BD3cXnt1aht7s%3D, PID: 10995464
  • Saito, K., Matsuda, F., Metabolomics for functional genomics, systems biology, and biotechnology (2010) Annual Review of Plant Biology, 61, pp. 463-489. , COI: 1:CAS:528:DC%2BC3cXnslSjsb4%3D, PID: 19152489
  • Sauvage, C., Segura, V., Bauchet, G., Stevens, R., Do, P.T., Nikoloski, Z., Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits (2014) Plant Physiology, 165 (3), pp. 1120-1132. , COI: 1:CAS:528:DC%2BC2cXhtFOqsbvN, PID: 24894148
  • Schauer, N., Fernie, A.R., Plant metabolomics: towards biological function and mechanism (2006) Trends in Plant Science, 11 (10), pp. 508-516. , COI: 1:CAS:528:DC%2BD28XhtVajsLzN, PID: 16949327
  • Schauer, N., Semel, Y., Balbo, I., Steinfath, M., Repsilber, D., Selbig, J., Mode of inheritance of primary metabolic traits in tomato (2008) The Plant Cell, 20 (3), pp. 509-523. , COI: 1:CAS:528:DC%2BD1cXlsl2ktLY%3D, PID: 18364465
  • Schauer, N., Semel, Y., Roessner, U., Gur, A., Balbo, I., Carrari, F., Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement (2006) Nature Biotechnology, 24 (4), pp. 447-454. , COI: 1:CAS:528:DC%2BD28Xjt1WisLg%3D, PID: 16531992
  • Schauer, N., Steinhauser, D., Strelkov, S., Schomburg, D., Allison, G., Moritz, T., GC-MS libraries for the rapid identification of metabolites in complex biological samples (2005) FEBS Letters, 579 (6), pp. 1332-1337. , COI: 1:CAS:528:DC%2BD2MXhslCjurs%3D, PID: 15733837
  • Schauer, N., Zamir, D., Fernie, A.R., Metabolic profiling of leaves and fruit of wild species tomato: a survey of the Solanum lycopersicum complex (2005) Journal of Experimental Botany, 56 (410), pp. 297-307. , COI: 1:CAS:528:DC%2BD2MXkt1Wltw%3D%3D, PID: 15596477
  • Schilmiller, A.L., Moghe, G.D., Fan, P., Ghosh, B., Ning, J., Jones, A.D., Functionally divergent alleles and duplicated loci encoding an acyltransferase contribute to acylsugar metabolite diversity in Solanum trichomes (2015) The Plant Cell, 27 (4), pp. 1002-1017. , COI: 1:CAS:528:DC%2BC2MXosFSis74%3D, PID: 25862303
  • Sonnewald, U., Fernie, A.R., Next-generation strategies for understanding and influencing source-sink relations in crop plants (2018) Current Opinion in Plant Biology, 43, pp. 63-70. , PID: 29428477
  • Steinhauser, M.C., Steinhauser, D., Gibon, Y., Bolger, M., Arrivault, S., Usadel, B., Identification of enzyme activity quantitative trait loci in a Solanum lycopersicum x Solanum pennellii introgression line population (2011) Plant Physiology, 157 (3), pp. 998-1014. , COI: 1:CAS:528:DC%2BC3MXhsFehur7O, PID: 21890649
  • Tieman, D., Zhu, G., Resende, M.F., Jr., Lin, T., Nguyen, C., Bies, D., A chemical genetic roadmap to improved tomato flavor (2017) Science, 355 (6323), pp. 391-394. , COI: 1:CAS:528:DC%2BC2sXhsVGrsb8%3D, PID: 28126817
  • Tieman, D.M., Zeigler, M., Schmelz, E.A., Taylor, M.G., Bliss, P., Kirst, M., Identification of loci affecting flavour volatile emissions in tomato fruits (2006) Journal of Experimental Botany, 57 (4), pp. 887-896. , COI: 1:CAS:528:DC%2BD28XitVOqtrY%3D, PID: 16473892
  • Tohge, T., Scossa, F., Fernie, A.R., Integrative approaches to enhance understanding of plant metabolic pathway structure and regulation (2015) Plant Physiology, 169 (3), pp. 1499-1511. , COI: 1:CAS:528:DC%2BC28Xjs1Khu7Y%3D, PID: 26371234
  • Toubiana, D., Batushansky, A., Tzfadia, O., Scossa, F., Khan, A., Barak, S., Combined correlation-based network and mQTL analyses efficiently identified loci for branched-chain amino acid, serine to threonine, and proline metabolism in tomato seeds (2015) The Plant Journal, 81 (1), pp. 121-133. , COI: 1:CAS:528:DC%2BC2cXitFGrsL%2FE, PID: 25359542
  • Toubiana, D., Semel, Y., Tohge, T., Beleggia, R., Cattivelli, L., Rosental, L., Metabolic profiling of a mapping population exposes new insights in the regulation of seed metabolism and seed, fruit, and plant relations (2012) PLoS Genetics, 8 (3)
  • Wen, W., Li, K., Alseekh, S., Omranian, N., Zhao, L., Zhou, Y., Genetic determinants of the network of primary metabolism and their relationships to plant performance in a maize recombinant inbred line population (2015) The Plant Cell, 27 (7), pp. 1839-1856. , COI: 1:CAS:528:DC%2BC2MXhsVOhtr%2FI, PID: 26187921
  • Xu, X., Martin, B., Comstock, J.P., Vision, T.J., Tauer, C.G., Zhao, B., Fine mapping a QTL for carbon isotope composition in tomato (2008) Theoretical and Applied Genetics, 117 (2), pp. 221-233. , COI: 1:CAS:528:DC%2BD1cXnslKlu78%3D, PID: 18542914
  • Ye, J., Wang, X., Hu, T., Zhang, F., Wang, B., Li, C., An InDel in the promoter of Al-activated malate transporter9 selected during tomato domestication determines fruit malate contents and aluminum tolerance (2017) The Plant Cell, 29 (9), pp. 2249-2268. , COI: 1:CAS:528:DC%2BC1cXhsFamurnN, PID: 28814642
  • Zanor, M.I., Rambla, J.L., Chaib, J., Steppa, A., Medina, A., Granell, A., Metabolic characterization of loci affecting sensory attributes in tomato allows an assessment of the influence of the levels of primary metabolites and volatile organic contents (2009) Journal of Experimental Botany, 60 (7), pp. 2139-2154. , COI: 1:CAS:528:DC%2BD1MXmtFSjtLc%3D, PID: 19346240
  • Zou, H., Hastie, T., (2012) Elastic-Net for Sparse Estimation and Sparse PCA, ,, Retrieved from


---------- APA ----------
Nunes-Nesi, A., Alseekh, S., de Oliveira Silva, F.M., Omranian, N., Lichtenstein, G., Mirnezhad, M., González, R.R.R.,..., Fernie, A.R. (2019) . Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds. Metabolomics, 15(4).
---------- CHICAGO ----------
Nunes-Nesi, A., Alseekh, S., de Oliveira Silva, F.M., Omranian, N., Lichtenstein, G., Mirnezhad, M., et al. "Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds" . Metabolomics 15, no. 4 (2019).
---------- MLA ----------
Nunes-Nesi, A., Alseekh, S., de Oliveira Silva, F.M., Omranian, N., Lichtenstein, G., Mirnezhad, M., et al. "Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds" . Metabolomics, vol. 15, no. 4, 2019.
---------- VANCOUVER ----------
Nunes-Nesi, A., Alseekh, S., de Oliveira Silva, F.M., Omranian, N., Lichtenstein, G., Mirnezhad, M., et al. Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds. Metabolomics. 2019;15(4).