Multi-year field trials provide a massive repository of trait data on a highly diverse population of tomato and uncover novel determinants of tomato productivity.
genome-wide association
soluble solids
tomato yield
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
21
04
2023
received:
01
12
2022
accepted:
29
04
2023
medline:
10
11
2023
pubmed:
8
5
2023
entrez:
8
5
2023
Statut:
ppublish
Résumé
Tomato (Solanum lycopersicum) is a prominent fruit with rich genetic resources for crop improvement. By using a phenotype-guided screen of over 7900 tomato accessions from around the world, we identified new associations for complex traits such as fruit weight and total soluble solids (Brix). Here, we present the phenotypic data from several years of trials. To illustrate the power of this dataset we use two case studies. First, evaluation of color revealed allelic variation in phytoene synthase 1 that resulted in differently colored or even bicolored fruit. Secondly, in view of the negative relationship between fruit weight and Brix, we pre-selected a subset of the collection that includes high and low Brix values in each category of fruit size. Genome-wide association analysis allowed us to detect novel loci associated with total soluble solid content and fruit weight. In addition, we developed eight F2 biparental intraspecific populations. Furthermore, by taking a phenotype-guided approach we were able to isolate individuals with high Brix values that were not compromised in terms of yield. In addition, the demonstration of novel results despite the high number of previous genome-wide association studies of these traits in tomato suggests that adoption of a phenotype-guided pre-selection of germplasm may represent a useful strategy for finding target genes for breeding.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1136-1151Subventions
Organisme : PlantaSYST
ID : 664621
Organisme : PlantaSYST
ID : 739582
Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Alseekh, S., Aharoni, A., Brotman, Y., Contrepois, K., D'Auria, J., Ewald, J.C. et al. (2021) Mass spectrometry-based metabolomics: a guide for annotation, quantification and best reporting practices. Nature Methods, 18, 747-756.
Anon. (2015) Growing access to phenotype data. Nature Genetics, 47, 99.
Aulchenko, Y.S., Ripke, S., Isaacs, A. & van Duijn, C.M. (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics (Oxford, England), 23, 1294-1296.
Barrantes, W., López-Casado, G., García-Martínez, S., Alonso, A., Rubio, F., Ruiz, J.J. et al. (2016) Exploring new alleles involved in tomato fruit quality in an introgression line library of Solanum pimpinellifolium. Frontiers in Plant Science, 7, 1172.
Barry, C.S., McQuinn, R.P., Chung, M.Y., Besuden, A. & Giovannoni, J.J. (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiology, 147, 179-187.
Bombarely, A., Menda, N., Tecle, I.Y., Buels, R.M., Strickler, S., Fischer-York, T. et al. (2011) The sol genomics network (solgenomics.Net): growing tomatoes using Perl. Nucleic Acids Research, 39, D1149-D1155.
Börner, A. (2012) Nickolai Ivanovich Vavilov and his footprint on plant genetic resources conservation in Gemany. SEL'SKOKHOZYAISTVENNAYA BIOLOGIA, 5, 20-30.
Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y. & Buckler, E.S. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics (Oxford, England), 23, 2633-2635.
Chakrabarti, M., Zhang, N., Sauvage, C., Muños, S., Blanca, J., Cañizares, J. et al. (2013) A cytochrome P450 regulates a domestication trait in cultivated tomato. Proceedings of the National Academy of Sciences of the United States of America, 110, 17125-17130.
Chen, J., Beauvoit, B., Génard, M., Colombié, S., Moing, A., Vercambre, G. et al. (2021) Modelling predicts tomatoes can be bigger and sweeter if biophysical factors and transmembrane transports are fine-tuned during fruit development. The New Phytologist, 230, 1489-1502.
Do, P.T., Prudent, M., Sulpice, R., Causse, M. & Fernie, A.R. (2010) The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiology, 154, 1128-1142.
Earl, D.A. & von Holdt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S. et al. (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One, 6, e19379.
Frary, A., Nesbitt, T.C., Grandillo, S., Knaap, E., Cong, B., Liu, J. et al. (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science (New York, N.Y.), 289, 85-88.
Fridman, E., Carrari, F., Liu, Y.S., Fernie, A.R. & Zamir, D. (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science (New York, N.Y.), 305, 1786-1789.
Fridman, E., Liu, Y., Carmel-Goren, L., Gur, A., Shoresh, M., Pleban, T. et al. (2002) Two tightly linked QTLs modify tomato sugar content via different physiological pathways. Molecular Genetics and Genomics, 266, 821-826.
Fulton, T.M., Chuunwongse, J. & Tanksley, S.D. (1995) Microprep protocol for extraction of DNA from tomato and other herbaceaous plants. Plant Molecular Biology Reporter, 13, 207-209.
Huang, J., Lu, G., Liu, L., Raihan, M.S., Xu, J., Jian, L. et al. (2020) The kernel size-related quantitative trait locus qKW9 encodes a Pentatricopeptide repeat protein that Aaffects photosynthesis and grain filling. Plant Physiology, 183, 1696-1709.
Isaacson, T., Ronen, G., Zamir, D. & Hirschberg, J. (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. The Plant Cell, 14, 333-342.
Krieger, U., Lippman, Z.B. & Zamir, D. (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nature Genetics, 42, 459-463.
Leong, B.J., Lybrand, D.B., Lou, Y.R., Fan, P., Schilmiller, A.L. & Last, R.L. (2019) Evolution of metabolic novelty: a trichome-expressed invertase creates specialized metabolic diversity in wild tomato. Science Advances, 5, eaaw3754.
Letunic, I. & Bork, P. (2007) Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics (Oxford, England), 23, 127-128.
Lipka, A.E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P.J. et al. (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics (Oxford, England), 28, 2397-2399.
Lippman, Z.B., Cohen, O., Alvarez, J.P., Abu-Abied, M., Pekker, I., Paran, I. et al. (2008) The making of a compound inflorescence in tomato and related nightshades. PLoS Biology, 6, e288.
Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1, 387-396.
Liu, Y.S., Gur, A., Ronen, G., Causse, M., Damidaux, R., Buret, M. et al. (2003) There is more to tomato fruit colour than candidate carotenoid genes. Plant Biotechnology Journal, 1, 195-207.
Mackay, I. & Powell, W. (2007) Methods for linkage disequilibrium mapping in crops. Trends in Plant Science, 12, 57-63.
Magwaza, L.S. & Opara, U.L. (2015) Analytical methods for determination of sugars and sweetness of horticultural products - a review. Scientia Horticulturae, 184, 179-192.
Mu, Q., Huang, Z., Chakrabarti, M., Illa-Berenguer, E., Liu, X., Wang, Y. et al. (2017) Fruit weight is controlled by cell size regulator encoding a novel protein that is expressed in maturing tomato fruits. PLoS Genetics, 13, e1006930.
Park, S.J., Jiang, K., Tal, L., Yichie, Y., Gar, O., Zamir, D. et al. (2014) Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nature Genetics, 46, 1337-1342.
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
Prudent, M., Causse, M., Génard, M., Tripodi, P., Grandillo, S. & Bertin, N. (2009) Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection. Journal of Experimental Botany, 60, 923-937.
Rodríguez-Leal, D., Lemmon, Z.H., Man, J., Bartlett, M.E. & Lippman, Z.B. (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell, 171, 470-480.e478.
Ronen, G., Carmel-Goren, L., Zamir, D. & Hirschberg, J. (2000) An alternative pathway to beta -carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. Proceedings of the National Academy of Sciences of the United States of America, 97, 11102-11107.
Sauvage, C., Segura, V., Bauchet, G., Stevens, R., Do, P.T., Nikoloski, Z. et al. (2014) Genome-wide Association in Tomato Reveals 44 candidate loci for fruit metabolic traits. Plant Physiology, 165, 1120-1132.
Schauer, N., Semel, Y., Roessner, U., Gur, A., Balbo, I., Carrari, F. et al. (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nature Biotechnology, 24, 447-454.
Semel, Y., Nissenbaum, J., Menda, N., Zinder, M., Krieger, U., Issman, N. et al. (2006) Overdominant quantitative trait loci for yield and fitness in tomato. Proceedings of the National Academy of Sciences of the United States of America, 103, 12981-12986.
Sim, S.C., Durstewitz, G., Plieske, J., Wieseke, R., Ganal, M.W., Van Deynze, A. et al. (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS One, 7, e40563.
Soyk, S., Lemmon, Z.H., Oved, M., Fisher, J., Liberatore, K.L., Park, S.J. et al. (2017) Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell, 169, 1142-1155.e1112.
Soyk, S., Lemmon, Z.H., Sedlazeck, F.J., Jiménez-Gómez, J.M., Alonge, M., Hutton, S.F. et al. (2019) Duplication of a domestication locus neutralized a cryptic variant that caused a breeding barrier in tomato. Nature Plants, 5, 471-479.
Szymański, J., Bocobza, S., Panda, S., Sonawane, P., Cárdenas, P.D., Lashbrooke, J. et al. (2020) Analysis of wild tomato introgression lines elucidates the genetic basis of transcriptome and metabolome variation underlying fruit traits and pathogen response. Nature Genetics, 52, 1111-1121.
Tam, V., Patel, N., Turcotte, M., Bossé, Y., Paré, G. & Meyre, D. (2019) Benefits and limitations of genome-wide association studies. Nature Reviews. Genetics, 20, 467-484.
Tanksley, S.D. (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. The Plant Cell, 16, S181-S189.
Tieman, D., Zhu, G., Resende, M.F., Jr., Lin, T., Nguyen, C., Bies, D. et al. (2017) A chemical genetic roadmap to improved tomato flavor. Science (New York, N.Y.), 355, 391-394.
van Eijk, M.J., Broekhof, J.L., van der Poel, H.J., Hogers, R.C., Schneiders, H., Kamerbeek, J. et al. (2004) SNPWave: a flexible multiplexed SNP genotyping technology. Nucleic Acids Research, 32, e47.
Wang, X., Gao, L., Jiao, C., Stravoravdis, S., Hosmani, P.S., Saha, S. et al. (2020) Genome of Solanum pimpinellifolium provides insights into structural variants during tomato breeding. Nature Communications, 11, 5817.
Yamamoto, E., Matsunaga, H., Onogi, A., Kajiya-Kanegae, H., Minamikawa, M., Suzuki, A. et al. (2016) A simulation-based breeding design that uses whole-genome prediction in tomato. Scientific Reports, 6, 19454.
Ye, J., Li, W., Ai, G., Li, C., Liu, G., Chen, W. et al. (2019) Genome-wide association analysis identifies a natural variation in basic helix-loop-helix transcription factor regulating ascorbate biosynthesis via D-mannose/L-galactose pathway in tomato. PLoS Genetics, 15, e1008149.
Ye, J., Wang, X., Hu, T., Zhang, F., Wang, B., Li, C. et al. (2017) An InDel in the promoter of Al-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. The Plant Cell, 29, 2249-2268.
Yoshiba, Y., Kiyosue, T., Nakashima, K., Yamaguchi-Shinozaki, K. & Shinozaki, K. (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant & Cell Physiology, 38, 1095-1102.
Young, P.A. (1956) Ry. A modifier gene for red color in yellow tomato fruit. Report of the - Tomato Genetics Cooperative, 33, 6.
Yuste-Lisbona, F.J., Fernández-Lozano, A., Pineda, B., Bretones, S., Ortíz-Atienza, A., García-Sogo, B. et al. (2020) ENO regulates tomato fruit size through the floral meristem development network. Proceedings of the National Academy of Sciences of the United States of America, 117, 8187-8195.
Zanor, M.I., Osorio, S., Nunes-Nesi, A., Carrari, F., Lohse, M., Usadel, B. et al. (2009) RNA interference of LIN5 in tomato confirms its role in controlling brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology, 150, 1204-1218.
Zhang, N., Brewer, M.T. & van der Knaap, E. (2012) Fine mapping of fw3.2 controlling fruit weight in tomato. Theoretical and Applied Genetics, 125, 273-284.
Zhu, G., Wang, S., Huang, Z., Zhang, S., Liao, Q., Zhang, C. et al. (2018) Rewiring of the fruit metabolome in tomato breeding. Cell, 172, 249-261.e212.