Abstract
Tomato is a model species for genetic analyses since a long time. Many mutations controlled by a single gene were discovered and the underlying genes were mapped first on the tomato genetic map. Most of these genes are involved in fruit colour and shape, in plant growth and architecture and in disease resistances. With the construction of high-density molecular genetic maps, many genes were located on the genome and subsequently several of them were fine-mapped and further identified by positional cloning. Today with the availability of the tomato genome sequence these genes are physically located on the genome and the identification of new ones is being considerably accelerated. The alignment of the physical and genetic maps allowed the identification of hot spots of recombination and of large regions where recombination is almost suppressed, whatever the progeny studied. The impact of this heterogeneity in recombination is discussed.
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Introduction
Tomato has been a model species for genetic analyses for years. The diversity of its fruit colour, shape and size has interested geneticists since the early work of genetic mapping. Butler (1952) proposed one of the first genetic maps including more than 50 loci corresponding to phenotypic mutations. Nevertheless, until the discovery of molecular markers in the late 1980s, the location of mutations on genetic maps was not really precise as it was impossible to simultaneously map many loci. Molecular markers have enabled biologists to construct saturated linkage maps of the genome and to systematically localize mutations of interest on these maps. Over years, more and more markers were discovered and the genotyping cost decreased. Following isozymes, the first DNA markers, based on the detection of Restriction Fragment Length Polymorphisms (RFLP), allowed the construction of a reference map of the tomato genome (Tanksley et al. 1992). With more than 1000 loci, spread on the 12 chromosomes, this map allowed the precise localization of several mutations and of a few genes of interest. New mutations or genes of interest were subsequently mapped using either F2 populations or pairs of near isogenic lines differing only in the region of the interesting gene (Laterrot 1996). Bulks of individuals were later used (following the Bulk Segregant Analysis method), together with markers based on PCR amplification of the DNA (RAPD or AFLP markers). Following the identification of PCR markers linked to the gene of interest, specific PCR markers were set up, simplifying the genotyping step for breeders. Nevertheless, PCR markers such as RAPD or AFLP are dominant and map for the most part close to the centromeres, reducing their potential efficiency for gene mapping in tomato (Grandillo and Tanksley 1996; Haanstra et al. 1999; Saliba-Colombani et al. 2000). Markers based on the variation in the number of small sequence repeats (microsatellites or SSR) were then discovered and mapped on the reference map or used for the construction of new maps (He et al. 2002; Liu et al. 2005). To increase the number of markers available and to use the microsynteny observed with the Arabidopsis thaliana genome, Fulton et al. (2002) proposed the use of Conserved Ortholog Sequences (COS) as markers.
The polymorphism revealed by RFLP markers among cultivated accessions was very low and only a few markers were polymorphic and thus useful for mapping genes in such genetic background (Saliba-Colombani et al. 2000). Interspecific progenies were much more polymorphic and maps based on progenies derived from crosses with every wild species related to tomato were constructed (Labate et al. 2007). A population of introgression lines derived from a cross with a Solanum pennellii accession (Eshed and Zamir 1995) was particularly useful to discover new genes and quantitative trait loci (QTL) involved in fruit colour, size and plant traits (Zamir 2001).
More recently, several tomato accessions were used to sequence fragments of expressed sequences and identify Expressed Sequence Tags (ESTs), allowing the first Single Nucleotide Polymorphism (SNP) markers to be discovered and mapped (Labate and Baldo 2005; Sim et al. 2009). With the access to the tomato genome sequence (Tomato Genome Consortium 2012), the increased throughput of sequencing and the advances in Next Generation Sequencing technologies, it has been possible to discover thousands of SNPs through RNA sequencing (RNAseq). The SolCAP consortium developed a SNP array carrying more than 8000 SNPs chosen to reveal polymorphisms among cultivated accessions (Sim et al. 2012). Another SNP array was developed by Víquez-Zamora et al. (2013). Today, thanks to the tomato genome sequence availability, several projects of resequencing whole genomes of tomato accessions allowed the discovery of several millions of SNP (Causse et al. 2013; Aflitos et al. 2014; Lin et al. 2014) and the construction of genetic maps at the intraspecific level is now possible (Shirasawa et al. 2010). Large SNP arrays permit the rapid mapping of new loci of interest (Viquez-Zamora et al. 2014).
Genes and Loci Involved in Morphological and Fruit Characteristics
Among the major mutations used in tomato, the self-pruning (sp) mutation was discovered about 100 years ago and confers the determinate growth behaviour. It was largely used in processing tomato for field grown production. The tomato SELF-PRUNING (SP) gene is the homolog of the Antirrhinum majus CENTRORADIALIS (CEN) and Arabidopsis thaliana TERMINAL FLOWER1 (TFL1) genes (Pnueli et al. 1998).
Many mutations in genes related to the carotenoid pathway were identified and correspond to specific fruit colours (Hirschberg 2001). Among them the B/ogc locus has been shown to correspond to two mutations in the same gene responsible for either yellow or dark red colour of the fruit (Ronen et al. 2000). Recently the gene conferring the uniform ripening (u) phenotype was cloned and shown to correspond to a Golden 2-like (GLK) transcription factor, which determines the chlorophyll accumulation and distribution in developing fruit (Powell et al. 2012). The y locus, responsible for the pink fruit colour (due to a colourless peel which lacks the yellow flavonoid pigment naringenin chalcone), was also cloned. It corresponds to a MYB transcription factor (Adato et al. 2009; Ballester et al. 2010). Several alleles and their polymorphisms were identified at the y locus, thanks to the recent resequencing of more than 300 tomato accessions (Lin et al. 2014). Several mutations confer a long shelf life to the fruit. The most widely used, rin (for ripening inhibitor) corresponds to a deletion in a MADS BOX transcription factor (Vrebalov et al. 2002). Another important discovery was the mutation at the Cnr locus (Colourless non-ripening), which was one of the first epiallele discovered in tomato (Manning et al. 2006). Table 3.1 lists the genes involved in morphological and fruit mutations.
Disease Resistance Genes
Tomato is susceptible to many pathogens and all the resistance genes (R) were discovered in wild relatives. Many tomato disease resistance genes were mapped and characterized (Table 3.2). Since the first positionally cloned R gene (Pto, by Martin et al. 1993), more than 20 genes were cloned and characterized. Their structure and evolution was analyzed and the great conservation among genes conferring resistance to different types of pathogens revealed. The majority of R genes cloned so far encode proteins with a nucleotide-binding site (NBS) and a leucine-rich repeat (LRR) region (Ellis et al. 2000).
Mutant Collections
Many natural mutations were discovered in tomato. The Tomato Genetic Resources Center (TGRC, Davis, California, USA) collection encompasses more than 1000 monogenic mutants at over 600 loci, including spontaneous and induced mutations affecting many aspects of plant development and morphology, disease resistance genes, protein marker stocks, and other traits of economic importance (Chetelat 2005). Genetic data on individual stocks, including phenotypes, images, chromosome locations, etc. are available at the TGRC website (http://tgrc.ucdavis.edu/).
An additional series of provisional (i.e. less well-characterized) mutants is also available. The Hebrew University of Jerusalem developed an isogenic mutant library in the genetic background of cv. M82 (http://zamir.sgn.cornell.edu/mutants/index.html). A total of 13,000 M2 families, generated by ethylmethane sulfonate (EMS) and fast-neutron mutagenesis, were phenotypically analyzed and catalogued into at least 3417 mutations (Menda et al. 2004). This series of mutations includes many previously described mutant phenotypes as well as many novel mutants, and multiple alleles per locus. Screening this collection allowed the discovery of interesting alleles which interact with the SP gene and whose mutation modify its expression and may allow optimization of crop productivity (Park et al. 2014). Other collections of mutants are available (Okabe et al. 2011). Together these mutant collections provide important tools for analyses of gene function either through forward or reverse genetic approaches (Chap. 5).
Recombination Heterogeneity
Many genes/mutations were mapped on a genetic map but not yet cloned (Table 3.3). The recent availability of the tomato genome sequence confirmed earlier observations that recombination is unevenly distributed along chromosomes and that large pieces of the chromosomes around the centromeres do not recombine at all (Sim et al. 2012; Tomato Genome Consortium 2012). If the recombination frequencies may vary from one progeny to the other (Fig. 3.1), these regions do not recombine more in any. The ratio of kb per cM thus greatly varies hampering the characterization of some mutations due to the lack of recombination. Hopefully, these regions of low recombination also correspond to regions with lower gene density.
Many genes involved in morphological traits or disease resistances remain to be characterized. The high-quality genome sequence and millions of SNPs available today constitute unique resources to rapidly identify new genes of interest. High throughput genotyping technologies combined to the information on gene annotation and expression in various tissues should make the task much easier.
References
Adato A, Mandel T, Mintz-Oron S et al (2009) Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genet 5:e1000777
Aflitos SA, Schijlen EGWM, de Jong JHSGM et al (2014) Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant J 80:136–148
Astua-Monge G, Minsavage GV, Stall RE et al (2000) Xv4-vrxv4: a new gene-for-gene interaction identified between Xanthomonas campestris pv. vesicatoria Race T3 and the wild tomato relative Lycopersicon pennellii. Mol Plant Microbe Interact 13:1346–1355
Bai Y, van der Hulst R, Huang CC et al (2004) Mapping Ol-4, a gene conferring resistance to Oidium neolycopersici and originating from Lycopersicon peruvianum LA2172, requires muliallelic, single-locus markers. Theor Appl Genet 109:1215–1223
Bai Y, van der Hulst R, Bonnema G et al (2005) Tomato defense to Oidium neolycopersici: dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. Mol Plant Microbe Interact 18(4):354–362
Bai Y, Pavan S, Zheng Z et al (2008) Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of Mlo function. Mol Plant Microbe Interact 21(1):30–39
Ballester AR, Molthoff J, de Vos R et al (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Phys 152:71–84
Ballvora A, Pierre M, van den Ackerveken G et al (2001) Genetic mapping and functional analysis of the tomato Bs4 locus governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs4 protein. Mol Plant Microbe Interact 14:629–638
Barry CS, Giovannoni JJ (2006) Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci USA 103(20):7923–7928
Barry CS, McQuinn RP, Chung MY et al (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 Physiol 147(1):179–187
Barry CS, Aldridge GM, Herzog G et al (2012) Altered chloroplast development and delayed fruit ripening caused by mutations in a zinc metalloprotease at the lutescent2 locus of tomato. Plant Physiol 159(3):1086–1098
Bassel GW, Mullen RT, Bewley JD (2008) procera is a putative DELLA mutant in tomato (Solanum lycopersicum): effects on the seed and vegetative plant. J Exp Bot 59(3):585–593
Behare J, Laterrot H, Sarfatti M et al (1991) Restriction fragment length polymorphisms mapping of the Stemphylium resistance gene in tomato. Mol Plant Microbe Interact 4:489–492
Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136(5):823–832
Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol 144(1):312–323
Bishop GJ, Harrison K, Jones JD (1996) The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell 8(6):959–969
Brommonschenkel SH, Frary A, Tanksley SD (2000) The broadspectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Mol Plant Microbe Interact 13:1130–1138
Budiman MA, Chang S-B, Lee S et al (2004) Localization of jointless-2 gene in the centromeric region of tomato chromosome 12 based on high resolution genetic and physical mapping. Theor Appl Genet 108:190–196
Burbidge A, Grieve TM, Jackson A et al (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17(4):427–431
Busch BL, Schmitz G, Rossmann S, Piron F, Ding J, Bendahmane A, Theres K (2011) Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. Plant Cell 23(10):3595–3609
Butler L (1952) The linkage map of the tomato. J Heredity 43:25–35
Causse M, Desplat N, Pascual L, Le Paslier MC, Sauvage C, Bauchet G et al (2013) Whole genome resequencing in tomato reveals variation associated with introgression and breeding events. BMC Genom 14:791
Chetelat RT (2005) Revised list of monogenic stocks. Rep Tomato Genet Coop 55:48–69
Chunwongse J, Bunn TB, Crossman C et al (1994) Chromosomal localization and molecular-marker tagging of the powdery mildew resistance gene (Lv) in tomato. Theor Appl Genet 89:76–79
Chunwongse S, Doganlar C, Crossman JJ et al (1997) High-resolution genetic map of the Lv resistance locus in tomato. Theor Appl Genet 95:220–223
David-Schwartz R, Koenig D, Sinha N (2009) LYRATE is a key regulator of leaflet initiation and lamina outgrowth in tomato. Plant Cell 21:3093–3104
De Giovanni C, Dell’Orco P, Bruno A et al (2004) Identification of PCR-based markers (RAPD, AFLP) linked to a novel powdery mildew resistance gene (ol-2) in tomato. Plant Sci 166:41–48
Dixon MS, Jones DA, Keddie JS et al (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–459
Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JD (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10(11):1915–1925
Doganlar S, Dodson J, Gabor B et al (1998) Molecular mapping of the py-1 gene for resistance to corky root rot (Pyrenochaeta lycopersici) in tomato. Theor Appl Genet 97:784–788
Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284
Ernst K, Kumar A, Kriseleit D et al (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31(2):127–136
Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield associated QTL. Genetics 141:1147–1162
Fray RG, Grierson D (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol 22(4):589–602
Fulton TM, van der Hoeven R, Eanetta NT et al (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467
Galpaz N, Ronen G, Khalfa Z, Zamir D et al (2006) A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18(8):1947–1960
Grandillo S, Tanksley SD (1996) Genetic analysis of RFLPs, GATA microsatellites and RAPDs in a cross between L. esculentum and L. pimpinellifolium. Theor Appl Genet 92:957–965
Haanstra JPW, Wye C, Verbakel H et al (1999) An integrated high-density RFLP-AFLP map of tomato based on two Lycopersicon esculentum × L. pennellii F2 populations. Theor Appl Genet 99:254–271. doi:10.1007/s001220051231
Haanstra JPW, Meijer-Dekens F, Laugé R et al (2000) Mapping strategy for resistance genes against Cladosporium fulvum on the short arm of chromosome 1 of tomato: Cf-ECP5 near the Hcr9 milky way cluster. Theor Appl Genet 101:661–668
He C, Poysa V, Yu K (2002) Development and characterization of simple sequence repeat (SSR) markers and their use in determining relationships among Lycopersicon esculentum cultivars. Theor Appl Genet 106:363–373
Hemming MN, Basuki S, McGrath DJ et al (2004) Fine mapping of the tomato I-3 gene for fusarium wilt resistance and elimination of a co-segregating resistance gene analogue as a candidate for I-3. Theor Appl Genet 109(2):409–418
Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218
Hovav R, Chehanovsky N, Moy M et al (2007) The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant J 52(4):627–639
Huang CC, Cui YY, Weng CR et al (2000a) Development of diagnostic PCR markers closely linked to the tomato powdery mildew resistance gene Ol-1 on chromosome 6 of tomato. Theor Appl Genet 101:918–924
Huang CC, Hoefs-Van De Putte PM, Haanstra-Van Der Meer JG et al (2000b) Characterization and mapping of resistance to Oidium lycopersicum in two Lycopersicon hirsutum accessions: evidence for close linkage of two Ol-genes on chromosome 6 of tomato. Heredity 85:511–520
Isaacson T, Ronen G, Zamir D et al (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. Plant Cell 14(2):333–342
Ishibashi K, Masuda K, Naito S et al (2007) An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proc Natl Acad Sci USA 104:13833–13838
Jablonska B, Ammiraju JSS, Bhattarai KK et al (2007) The Mi-9 gene from Solanum arcanum conferring heat-stable resistance to root-knot nematodes is a homolog of Mi-1. Plant Physiol 143:1044–1054
Jones DA, Dickinson MJ, Balint-Kurti PJ et al (1993) Two complex resistance loci revealed in tomato by classical and RFLP mapping of the Cf-2, Cf-4, Cf-5, and Cf-9 genes for resistance to Cladosporium fulvum. Mol Plant Microbe Interact 6:348–357
Jones DA, Thomas CM, Hammond-Kosack KE et al (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793
Josse EM, Simkin AJ, Gaffé J et al (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol 123(4):1427–1436
Kaloshian I, Yaghoobi J, Liharska T et al (1998) Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol Gen Genet 257(3):376–385
Katsir L, Schilmiller AL, Staswick PE et al (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105(19):7100–7105
Kawchuk LM, Hachey J, Lynch DR et al (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98(11):6511–6515
Kinzer SM, Schwager SJ, Mutschler MA (1990) Mapping of ripening-related or -specific cDNA clones of tomato (Lycopersicon esculentum). Theor Appl Genet 79:489–496
Kondo K, Yamamoto M, Matton DPY et al (2002) Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of self-incompatibility. Plant J 29(5):627–636
Labate JA, Baldo AM (2005) Tomato SNP discovery by EST mining and resequencing. Mol Breed 16:343–349
Labate JA, Grandillo S, Fulton T et al (2007) Tomato. In: Kole C (ed) Genome mapping and molecular breeding in plants, vol 5, Vegetables. Springer, Berlin, pp 11–135
Lanfermeijer FC, Dijkhuis J, Sturre MJ et al (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon esculentum. Plant Mol Biol 52(5):1037–1049
Laterrot H (1996) Stock List. Rep Tom Genet Coop 46:34
Lieberman M, Segev O, Gilboa N et al (2004) The tomato homolog of the gene encoding UV-damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. Theor Appl Genet 108(8):1574–1581
Lim GT, Wang GP, Hemming MN et al (2008) High resolution genetic and physical mapping of the I-3 region of tomato chromosome 7 reveals almost continuous microsynteny with grape chromosome 12 but interspersed microsynteny with duplications on Arabidopsis chromosomes 1, 2 and 3. Theor Appl Genet 118(1):57–75
Lin T, Zhu G, Zhang J et al (2014) Genomic analyses provide insights into the history of tomato breeding. Nat Genet 46:1220–1226
Ling HQ, Koch G, Bäumlein H et al (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96(12):7098–7103
Ling HQ, Bauer P, Bereczky Z et al (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99(21):13938–13943
Lippman ZB, Cohen O, Alvarez JP et al (2008) The making of a compound inflorescence in tomato and related nightshades. PLoS Biol 11:e288
Liu Y, Roof S, Ye Z et al (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Nat Acad Sci USA 101:9897–9902
Liu Y, Chen H, Wei Y et al (2005) Construction of a genetic map and localization of QTLs for yield traits in tomato by SSR markers. Prog Nat Sci 15:793–797
Manning K, Tör M, Poole M et al (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38(8):948–952
Mao L, Begum D, Chuang HW et al (2000) JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406(6798):910–913
Martin GB, Brommonschenkel S, Chunwongse J et al (1993) Map-based cloning of a protein-kinase gene conferring disease resistance in tomato. Science 262:1432–1436
Martin GB, Frary A, Wu T et al (1994) A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6(11):1543–1552
Martín-Trillo M, Grandío EG, Serra F et al (2011) Role of tomato BRANCHED1-like genes in the control of shoot branching. Plant J 67(4):701–714
Menda N, Semel Y, Peled D et al (2004) In silico screening of a saturated mutation library of tomato. Plant J 38:861–872
Mesbah LA, Kneppers TJ, Takken FL et al (1999) Genetic and physical analysis of a YAC contig spanning the fungal disease resistance locus Asc of tomato (Lycopersicon esculentum). Mol Gen Genet 261(1):50–57
Molinero-Rosales N, Jamilena M, Zurita S et al (1999) FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J 20(6):685–693
Molinero-Rosales N, Latorre A, Jamilena M et al (2004) SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta 218(3):427–434
Montoya T, Nomura T, Farrar K et al (2002) Cloning the tomato curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14(12):3163–3176
Moore S, Vrebalov J, Payton P et al (2002) Use of genomics tools to isolate key ripening genes and analyse fruit maturation in tomato. J Exp Bot 53(377):2023–2030
Moreau P, Thoquet P, Olivier J et al (1998) Genetic Mapping of Ph-2, a single locus controlling partial resistance to Phytophthora infestans in tomato. Mol Plant Microbe Interact 11(4):259–269
Muramoto T, Kami C, Kataoka H et al (2005) The tomato photomorphogenetic mutant, aurea, is deficient in phytochromobilin synthase for phytochrome chromophore biosynthesis. Plant Cell Physiol 46(4):661–665
Mustilli AC, Fenzi F, Ciliento R et al (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11:145–157
Nashilevitz S, Melamed-Bessudo C, Aharoni A et al (2009) The legwd mutant uncovers the role of starch phosphorylation in pollen development and germination in tomato. Plant J 57(1):1–13
Okabe Y, Asamizu E, Saito T et al (2011) Tomato TILLING technology: development of a reverse genetics tool for the efficient isolation of mutants from Micro-Tom mutant libraries. Plant Cell Physiol 52(11):1994–2005
Ori N, Eshed Y, Paran I et al (1997) The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9(4):521–532
Ori N, Cohen AR, Etzioni A et al (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39(6):787–791
Park SJ, Jiang K, Tal L et al (2014) Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nat Genet 46(12):1337–1342
Parnis A, Cohen O, Gutfinger T et al (1997) The dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9(12):2143–2158
Parrella G, Ruffel S, Moretti A et al (2002a) Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes. Theor Appl Genet 105(6-7):855–861
Parrella G, Ruffel S, Moretti A et al (2002b) Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes. Theor Appl Genet 105(6-7):855–861
Parrella G, Moretti A, Gognalons P et al (2004) The Am gene controlling resistance to Alfalfa mosaic virus in tomato is located in the cluster of dominant resistance genes on chromosome 6. Phytopathology 94:345–350
Piron F, Nicolaï M, Minoïa S et al (2010) An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS ONE 5(6):e11313
Pnueli L, Carmel-Goren L, Hareven D et al (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989
Powell AL, Nguyen CV, Hill T et al (2012) Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336(6089):1711–1715
Rivers BA, Bernatzky R, Robinson SJ et al (1993) Molecular diversity at the self-incompatibility locus is a salient feature in natural populations of wild tomato (Lycopersicon peruvianum). Mol Gen Genet 238(3):419–427
Ronen GL, Cohen M, Zamir D et al (1999) Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J 17:341–351
Ronen G, Carmel-Goren L, Zamir D et al (2000) An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc Nat Acad Sci USA 97:11102–11107
Ruffel S, Gallois JL, Lesage ML et al (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Gen Genomics 274:346–353
Sagi M, Scazzocchio C, Fluhr R (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J 31(3):305–317
Saliba-Colombani V, Causse M, Gervais L et al (2000) Efficiency of RFLP, RAPD, and AFLP markers for the construction of an intraspecific map of the tomato genome. Genome 43:29–40
Salmeron J, Oldroyd G, Rommens C et al (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123–133
Sarfatti M, Abu-Abied M, Katan J et al (1991) RFLP mapping of I1, a new locus in tomato conferring resistance against Fusarium oxysporum f. sp. lycopersici race 1. Theor Appl Genet 82:22–26
Sato T, Iwatsubo T, Takahashi M et al (1993) Intercellular localization of acid invertase in tomato fruit and molecular cloning of a cDNA for the enzyme. Plant Cell Physiol 34(2):263–269
Schmitz G, Tillmann E, Carriero F et al (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc Natl Acad Sci USA 99(2):1064–1069
Schornack S, Ballvora A, Gürlebeck D et al (2004) The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37(1):46–60 Erratum in: Plant J 37(5):787
Schumacher K, Schmitt T, Rossberg M et al (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96(1):290–295
Scott JW, Agrama HA, Jones JP (2004) RFLP-based analysis of recombination among resistance genes to Fusarium wilt races 1, 2, and 3 in tomato. J Am Soc Hortic Sci 129:394–400
Sela-Buurlage MB, Budai-Hadrian O, Pan Q, Zamir D, Fluhr R (2001) Genome-wide dissection of Fusarium resistance in tomato reveals multiple complex loci. Mol Gen Genet 265:1104–1111
Shirasawa K, Isobe S, Hirakawa H et al (2010) SNP discovery and linkage map construction in cultivated tomato. DNA Res 17(6):381–391
Sim SC, Robbins MD, Chilcott C et al (2009) Oligonucleotide array discovery of polymorphisms in cultivated tomato (Solanum lycopersicum L.) reveals patterns of SNP variation associated with breeding. BMC Genom 10:466
Sim S-C, Durstewitz G, Plieske J et al (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE 7(7):e40563
Soumpourou E, Iakovidis M, Chartrain L et al (2007) The Solanum pimpinellifolium Cf-ECP1 and Cf-ECP4 genes for resistance to Cladosporium fulvum are located at the Milky Way locus on the short arm of chromosome 1. Theor Appl Genet 115:1127–1136
Stamova BS, Chetelat RT (2000) Inheritance and genetic mapping of cucumber mosaic virus resistance introgressed from Lycopersicon chilense into tomato. Theor Appl Genet 101:527–537
Tanksley SD, Loaiza-Figueroa F (1985) Gametophytic self-incompatibility is controlled by a single major locus on chromosome 1 in Lycopersicon peruvianum. Genetics 82:5093–5096
Tanksley SD, Ganal MW, Prince JP et al (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160
Terry MJ, Kendrick RE (1996) The aurea and yellow-green-2 mutants of tomato are deficient in phytochrome chromophore synthesis. J Biol Chem 271(35):21681–21686
Thomas CM, Jones DA, Parniske M et al (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209–2224
Thompson AJ, Jackson AC, Parker RA et al (2000) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol 42(6):833–845
Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400):635–641
Vakalounakis DJ, Laterrot H, Moretti A et al (1997) Linkage between Frl (Fusarium oxysporum f.sp. radicis-lycopersici resistance) and Tm-2 (tobacco mosaic virus resistance-2) loci in tomato (Lycopersicon esculentum). Ann Appl Biol 130:319–323
van der Biezen EA, Brandwagt BF, van Leeuwen W et al (1996) Identification and isolation of the FEEBLY gene from tomato by transposon tagging. Mol Gen Genet 251(3):267–280
Verlaan MG, Hutton SF, Ibrahem RM et al (2013) The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-Class RNA–dependent RNA polymerases. PLoS Genet 9(3):e1003399
Víquez-Zamora M, Vosman B, van de Geest H et al (2013) Tomato breeding in the genomics era: insights from a SNP array. BMC Genom 14:354
Viquez-Zamora AM, Caro Rios CM, Finkers R et al (2014) Mapping in the era of sequencing: high density genotyping and its application for mapping TYLCV resistance in Solanum pimpinellifolium. BMC Genom 15:1152. doi:10.1186/1471-2164-15-1152
Vrebalov J, Ruezinsky D, Padmanabhan V et al (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296(5566):343–346
Weller JL, Perrotta G, Schreuder ME et al (2001) Genetic dissection of blue-light sensing in tomato using mutants deficient in cryptochrome 1 and phytochromes A, B1 and B2. Plant J 25(4):427–440
Wilkinson JQ, Lanahan MB, Yen HC et al (1995) An ethylene-inducible component of signal transduction encoded by never-ripe. Science 270(5243):1807–1809
Yaghoobi J, Kaloshian I, Wen Y et al (1995) Mapping a new nematode resistance locus in Lycopersicon peruvianum. Theor Appl Genet 91:457–464
Yang C, Li H, Zhang J et al (2011) A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci USA 108(29):11836–11841
Yu ZH, Wang JF, Stall RE et al (1995) Genomic localization of tomato genes that control a hypersensitive reaction to Xanthomonas campestris pv. vesicatoria (Doidge) dye. Genetics 141(2):675–682
Yuan YN, Haanstra J, Lindhout P et al (2002) The Cladopsorium fulvum resistance gene Cf-ECP3 is part of the Orion cluster on the short arm of chromosome 1. Mol Breed 10:45–50
Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989
Zhang C, Liu L, Wang X et al (2014) The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to Phytophthora infestans. Theor Appl Genet 127(6):1353–1364
Zhang C, Liu L, Zheng Z et al (2013) Fine mapping of the Ph-3 gene conferring resistance to late blight (Phytophthora infestans) in tomato. Theor Appl Genet 126(10):2643–2653
Zhang J, Chen R, Xiao J et al (2007) A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant. J Plant Res 120(6):671–678
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Causse, M., Grandillo, S. (2016). Gene Mapping in Tomato. In: Causse, M., Giovannoni, J., Bouzayen, M., Zouine, M. (eds) The Tomato Genome. Compendium of Plant Genomes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-53389-5_3
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