A candidate gene survey of quantitative trait loci affecting chemical composition in tomato fruit

In tomato, numerous wild-related species have been demonstrated to be untapped sources of valuable genetic variability, including pathogen-resistance genes, nutritional, and industrial quality traits. From a collection of S. pennellii introgressed lines, 889 fruit metabolic loci (QML) and 326 yield-associated loci (YAL), distributed across the tomato genome, had been identified previously. By using a combination of molecular marker sequence analysis, PCR amplification and sequencing, analysis of allelic variation, and evaluation of co-response between gene expression and metabolite composition traits, the present report, provides a comprehensive list of candidate genes co-localizing with a subset of 106 QML and 20 YAL associated either with important agronomic or nutritional characteristics. This combined strategy allowed the identification and analysis of 127 candidate genes located in 16 regions of the tomato genome. Eighty-five genes were cloned and partially sequenced, totalling 45 816 and 45 787 bases from S. lycopersicum and S. pennellii, respectively. Allelic variation at the amino acid level was confirmed for 37 of these candidates. Furthermore, out of the 127 gene-metabolite co-locations, some 56 were recovered following correlation of parallel transcript and metabolite profiling. Results obtained here represent the initial steps in the integration of genetic, genomic, and expressional patterns of genes co-localizing with chemical compositional traits of the tomato fruit.

[1]  Sudhir Kumar,et al.  MEGA2: molecular evolutionary genetics analysis software , 2001, Bioinform..

[2]  F. Corpet Multiple sequence alignment with hierarchical clustering. , 1988, Nucleic acids research.

[3]  Z. Ye,et al.  Cloning and mapping of genes involved in tomato ascorbic acid biosynthesis and metabolism , 2006 .

[4]  M. Causse,et al.  Candidate Genes and Quantitative Trait Loci Affecting Fruit Ascorbic Acid Content in Three Tomato Populations , 2007, Plant Physiology.

[5]  R. Myers,et al.  Candidate-gene approaches for studying complex genetic traits: practical considerations , 2002, Nature Reviews Genetics.

[6]  Lukas A. Mueller,et al.  The Tomato Sequencing Project, the First Cornerstone of the International Solanaceae Project (SOL) , 2005, Comparative and functional genomics.

[7]  W. Kim,et al.  Expression of MdCAS1 and MdCAS2, encoding apple β-cyanoalanine synthase homologs, is concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus domestica Borkh.) fruits , 2007, Plant Cell Reports.

[8]  P. Quick,et al.  Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. , 2005, Plant & cell physiology.

[9]  Z. Lippman,et al.  An integrated view of quantitative trait variation using tomato interspecific introgression lines. , 2007, Current opinion in genetics & development.

[10]  G. Galili,et al.  Regulatory Role of Cystathionine-γ-Synthase and de novo Synthesis of Methionine in Ethylene Production during tomato Fruit Ripening , 2006, Plant Molecular Biology.

[11]  I. Paran,et al.  Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. , 2007, Journal of experimental botany.

[12]  S. Salvi,et al.  To clone or not to clone plant QTLs: present and future challenges. , 2005, Trends in plant science.

[13]  M. Oortwijn,et al.  Differences in regulation of carbohydrate metabolism during early fruit development between domesticated tomato and two wild relatives , 2007, Planta.

[14]  S. Miao,et al.  The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones , 2006, Cellular and Molecular Life Sciences CMLS.

[15]  M. Zanor,et al.  Integrated Analysis of Metabolite and Transcript Levels Reveals the Metabolic Shifts That Underlie Tomato Fruit Development and Highlight Regulatory Aspects of Metabolic Network Behavior1[W] , 2006, Plant Physiology.

[16]  T. C. Nesbitt,et al.  fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. , 2000, Science.

[17]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[18]  Li Li,et al.  The Cauliflower Or Gene Encodes a DnaJ Cysteine-Rich Domain-Containing Protein That Mediates High Levels of β-Carotene Accumulation[W] , 2006, The Plant Cell Online.

[19]  J. Selbig,et al.  Parallel analysis of transcript and metabolic profiles: a new approach in systems biology , 2003, EMBO reports.

[20]  B. Neel,et al.  Genetic and cellular mechanisms of oncogenesis , 2007 .

[21]  A. Bacic Breaking an impasse in pectin biosynthesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  F. Carrari,et al.  Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. , 2006, The Plant journal : for cell and molecular biology.

[23]  P. Green,et al.  Consed: a graphical tool for sequence finishing. , 1998, Genome research.

[24]  D. Zamir,et al.  An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. , 1995, Genetics.

[25]  Debra Mohnen,et al.  Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Thomas L. Madden,et al.  BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. , 1999, FEMS microbiology letters.

[27]  Alisdair R Fernie,et al.  Plant metabolomics: towards biological function and mechanism. , 2006, Trends in plant science.

[28]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[29]  A. Fernie,et al.  Natural genetic variation for improving crop quality. , 2006, Current opinion in plant biology.

[30]  G. Martin,et al.  Deductions about the Number, Organization, and Evolution of Genes in the Tomato Genome Based on Analysis of a Large Expressed Sequence Tag Collection and Selective Genomic Sequencing Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010478. , 2002, The Plant Cell Online.

[31]  Ruth E. Hartley,et al.  An integrated view. , 1973 .

[32]  F. Carrari,et al.  Enhanced Photosynthetic Performance and Growth as a Consequence of Decreasing Mitochondrial Malate Dehydrogenase Activity in Transgenic Tomato Plants1 , 2005, Plant Physiology.

[33]  J. Whitlock GENETIC AND MOLECULAR , 1990 .

[34]  D. Zamir,et al.  A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. , 2004, Journal of experimental botany.

[35]  S. Tanksley,et al.  Changes in Regulation of a Transcription Factor Lead to Autogamy in Cultivated Tomatoes , 2007, Science.

[36]  M. Ganal,et al.  Sequencing of cDNA clones from the genetic map of tomato (Lycopersicon esculentum). , 1998, Genome research.

[37]  D. Zamir,et al.  A Chromoplast-Specific Carotenoid Biosynthesis Pathway Is Revealed by Cloning of the Tomato white-flower Locus[W] , 2006, The Plant Cell Online.

[38]  F. Carrari,et al.  Zooming In on a Quantitative Trait for Tomato Yield Using Interspecific Introgressions , 2004, Science.

[39]  Mark H. Wright,et al.  The SOL Genomics Network. A Comparative Resource for Solanaceae Biology and Beyond1 , 2005, Plant Physiology.

[40]  U. Roessner,et al.  Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement , 2006, Nature Biotechnology.

[41]  Robert M. Buels,et al.  The SGN comparative map viewer , 2008, Bioinform..

[42]  Yoshihiro Yamanishi,et al.  KEGG for linking genomes to life and the environment , 2007, Nucleic Acids Res..

[43]  A. Price,et al.  Believe it or not, QTLs are accurate! , 2006, Trends in plant science.

[44]  P. Rey,et al.  The Arabidopsis Plastidic Methionine Sulfoxide Reductase B Proteins. Sequence and Activity Characteristics, Comparison of the Expression with Plastidic Methionine Sulfoxide Reductase A, and Induction by Photooxidative Stress , 2005, Plant Physiology.