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1.  Light-induced vegetative anthocyanin pigmentation in Petunia 
Journal of Experimental Botany  2009;60(7):2191-2202.
The Lc petunia system, which displays enhanced, light-induced vegetative pigmentation, was used to investigate how high light affects anthocyanin biosynthesis, and to assess the effects of anthocyanin pigmentation upon photosynthesis. Lc petunia plants displayed intense purple anthocyanin pigmentation throughout the leaves and stems when grown under high-light conditions, yet remain acyanic when grown under shade conditions. The coloured phenotypes matched with an accumulation of anthocyanins and flavonols, as well as the activation of the early and late flavonoid biosynthetic genes required for flavonol and anthocyanin production. Pigmentation in Lc petunia only occurred under conditions which normally induce a modest amount of anthocyanin to accumulate in wild-type Mitchell petunia [Petunia axillaris×(Petunia axillaris×Petunia hybrida cv. ‘Rose of Heaven’)]. Anthocyanin pigmentation in Lc petunia leaves appears to screen underlying photosynthetic tissues, increasing light saturation and light compensation points, without reducing the maximal photosynthetic assimilation rate (Amax). In the Lc petunia system, where the bHLH factor Leaf colour is constitutively expressed, expression of the bHLH (Lc) and WD40 (An11) components of the anthocyanin regulatory system were not limited, suggesting that the high-light-induced anthocyanin pigmentation is regulated by endogenous MYB transcription factors.
doi:10.1093/jxb/erp097
PMCID: PMC2682507  PMID: 19380423
Anthocyanin; bHLH; flavonol; Lc; Leaf colour; light; MYB; photosynthesis; vegetative pigmentation
2.  Genome-wide identification and functional analyses of calmodulin genes in Solanaceous species 
BMC Plant Biology  2013;13:70.
Background
Calmodulin (CaM) is a major calcium sensor in all eukaryotes. It binds calcium and modulates the activity of a wide range of downstream proteins in response to calcium signals. However, little is known about the CaM gene family in Solanaceous species, including the economically important species, tomato (Solanum lycopersicum), and the gene silencing model plant, Nicotiana benthamiana. Moreover, the potential function of CaM in plant disease resistance remains largely unclear.
Results
We performed genome-wide identification of CaM gene families in Solanaceous species. Employing bioinformatics approaches, multiple full-length CaM genes were identified from tomato, N. benthamiana and potato (S. tuberosum) genomes, with tomato having 6 CaM genes, N. benthamiana having 7 CaM genes, and potato having 4 CaM genes. Sequence comparison analyses showed that three tomato genes, SlCaM3/4/5, two potato genes StCaM2/3, and two sets of N. benthamiana genes, NbCaM1/2/3/4 and NbCaM5/6, encode identical CaM proteins, yet the genes contain different intron/exon organization and are located on different chromosomes. Further sequence comparisons and gene structural and phylogenetic analyses reveal that Solanaceous species gained a new group of CaM genes during evolution. These new CaM genes are unusual in that they contain three introns in contrast to only a single intron typical of known CaM genes in plants. The tomato CaM (SlCaM) genes were found to be expressed in all organs. Prediction of cis-acting elements in 5' upstream sequences and expression analyses demonstrated that SlCaM genes have potential to be highly responsive to a variety of biotic and abiotic stimuli. Additionally, silencing of SlCaM2 and SlCaM6 altered expression of a set of signaling and defense-related genes and resulted in significantly lower resistance to Tobacco rattle virus and the oomycete pathogen, Pythium aphanidermatum.
Conclusions
The CaM gene families in the Solanaceous species tomato, N. benthamiana and potato were identified through a genome-wide analysis. All three plant species harbor a small set of genes that encode identical CaM proteins, which may manifest a strategy of plants to retain redundancy or enhanced quantitative gene function. In addition, Solanaceous species have evolved one new group of CaM genes during evolution. CaM genes play important roles in plant disease resistance to a variety of pathogens.
doi:10.1186/1471-2229-13-70
PMCID: PMC3751459  PMID: 23621884
Calcium; Calmodulin; Gene Structure; Phylogenetic Analysis; Defense; Resistance; Tomato; Nicotiana Benthamiana; Potato
3.  Metabolic Engineering of Anthocyanin Biosynthesis in Escherichia coli 
Anthocyanins are red, purple, or blue plant pigments that belong to the family of polyphenolic compounds collectively called flavonoids. Their demonstrated antioxidant properties and economic importance to the dye, fruit, and cut-flower industries have driven intensive research into their metabolic biosynthetic pathways. In order to produce stable, glycosylated anthocyanins from colorless flavanones such as naringenin and eriodictyol, a four-step metabolic pathway was constructed that contained plant genes from heterologous origins: flavanone 3β-hydroxylase from Malus domestica, dihydroflavonol 4-reductase from Anthurium andraeanum, anthocyanidin synthase (ANS) also from M. domestica, and UDP-glucose:flavonoid 3-O-glucosyltransferase from Petunia hybrida. Using two rounds of PCR, each one of the four genes was first placed under the control of the trc promoter and its own bacterial ribosome-binding site and then cloned sequentially into vector pK184. Escherichia coli cells containing the recombinant plant pathway were able to take up either naringenin or eriodictyol and convert it to the corresponding glycosylated anthocyanin, pelargonidin 3-O-glucoside or cyanidin 3-O-glucoside. The produced anthocyanins were present at low concentrations, while most of the metabolites detected corresponded to their dihydroflavonol precursors, as well as the corresponding flavonols. The presence of side product flavonols is at least partly due to an alternate reaction catalyzed by ANS. This is the first time plant-specific anthocyanins have been produced from a microorganism and opens up the possibility of further production improvement by protein and pathway engineering.
doi:10.1128/AEM.71.7.3617-3623.2005
PMCID: PMC1169036  PMID: 16000769
4.  Molecular Characterization of Tomato Leaf Curl China Virus, Infecting Tomato Plants in China, and Functional Analyses of Its Associated Betasatellite▿† 
A novel tomato-infecting begomovirus from Guangxi province, China, was identified and characterized, for which the name Tomato leaf curl China virus (ToLCCNV) was proposed. Phylogenetic and recombination analyses of the virus genomic sequences suggested that ToLCCNV may have arisen by recombination among Tomato leaf curl Vietnam virus (ToLCVV), Tomato leaf curl Gujarat virus (ToLCGV), and an unknown virus. A betasatellite molecule was found to be associated with ToLCCNV (ToLCCNB), and its complete nucleotide sequences were determined. Infectious clones of ToLCCNV and ToLCCNB were constructed and then used for agro-inoculation of plants; ToLCCNV alone infected Nicotiana benthamiana, Nicotiana glutinosa, Petunia hybrida, and Solanum lycopersicum plants, but no symptoms were induced. ToLCCNB was required for induction of leaf curl disease in these hosts. The βC1 protein of ToLCCNB was identified as a suppressor of RNA silencing and accumulated primarily in the nucleus. Deletion mutagenesis of βC1 showed that the central part of βC1 (amino acids 44 to 74) was responsible for both the suppressor activity and nuclear localization.
doi:10.1128/AEM.00017-11
PMCID: PMC3126389  PMID: 21378048
5.  Evidence of cryptic introgression in tomato (Solanum lycopersicum L.) based on wild tomato species alleles 
BMC Plant Biology  2012;12:133.
Background
Many highly beneficial traits (e.g. disease or abiotic stress resistance) have been transferred into crops through crosses with their wild relatives. The 13 recognized species of tomato (Solanum section Lycopersicon) are closely related to each other and wild species genes have been extensively used for improvement of the crop, Solanum lycopersicum L. In addition, the lack of geographical barriers has permitted natural hybridization between S. lycopersicum and its closest wild relative Solanum pimpinellifolium in Ecuador, Peru and northern Chile. In order to better understand patterns of S. lycopersicum diversity, we sequenced 47 markers ranging in length from 130 to 1200 bp (total of 24 kb) in genotypes of S. lycopersicum and wild tomato species S. pimpinellifolium, Solanum arcanum, Solanum peruvianum, Solanum pennellii and Solanum habrochaites. Between six and twelve genotypes were comparatively analyzed per marker. Several of the markers had previously been hypothesized as carrying wild species alleles within S. lycopersicum, i.e., cryptic introgressions.
Results
Each marker was mapped with high confidence (e<1 x 10-30) to a single genomic location using BLASTN against tomato whole genome shotgun chromosomes (SL2.40) database. Neighbor-joining trees showed high mean bootstrap support (86.8 ± 2.34%) for distinguishing red-fruited from green-fruited taxa for 38 of the markers. Hybridization and parsimony splits networks, genomic map positions of markers relative to documented introgressions, and historical origins of accessions were used to interpret evolutionary patterns at nine markers with putatively introgressed alleles.
Conclusion
Of the 47 genetic markers surveyed in this study, four were involved in linkage drag on chromosome 9 during introgression breeding, while alleles at five markers apparently originated from natural hybridization with S. pimpinellifolium and were associated with primitive genotypes of S. lycopersicum. The positive identification of introgressed genes within crop species such as S. lycopersicum will help inform conservation and utilization of crop germplasm diversity, for example, facilitating the purging of undesirable linkage drag or the exploitation of novel, favorable alleles.
doi:10.1186/1471-2229-12-133
PMCID: PMC3462117  PMID: 22871151
Cryptic introgression; Linkage drag; Breeding; DNA sequence; Solanum species
6.  Coexpression Analysis of Tomato Genes and Experimental Verification of Coordinated Expression of Genes Found in a Functionally Enriched Coexpression Module 
Gene-to-gene coexpression analysis is a powerful approach to infer the function of uncharacterized genes. Here, we report comprehensive identification of coexpression gene modules of tomato (Solanum lycopersicum) and experimental verification of coordinated expression of module member genes. On the basis of the gene-to-gene correlation coefficient calculated from 67 microarray hybridization data points, we performed a network-based analysis. This facilitated the identification of 199 coexpression modules. A gene ontology annotation search revealed that 75 out of the 199 modules are enriched with genes associated with common functional categories. To verify the coexpression relationships between module member genes, we focused on one module enriched with genes associated with the flavonoid biosynthetic pathway. A non-enzyme, non-transcription factor gene encoding a zinc finger protein in this module was overexpressed in S. lycopersicum cultivar Micro-Tom, and expression levels of flavonoid pathway genes were investigated. Flavonoid pathway genes included in the module were up-regulated in the plant overexpressing the zinc finger gene. This result demonstrates that coexpression modules, at least the ones identified in this study, represent actual transcriptional coordination between genes, and can facilitate the inference of tomato gene function.
doi:10.1093/dnares/dsq002
PMCID: PMC2853382  PMID: 20130013
coexpression; flavonoid; Solanum lycopersicum; tomato; zinc finger
7.  Whole genome profiling physical map and ancestral annotation of tobacco Hicks Broadleaf 
The Plant Journal  2013;75(5):880-889.
Genomics-based breeding of economically important crops such as banana, coffee, cotton, potato, tobacco and wheat is often hampered by genome size, polyploidy and high repeat content. We adapted sequence-based whole-genome profiling (WGP™) technology to obtain insight into the polyploidy of the model plant Nicotiana tabacum (tobacco). N. tabacum is assumed to originate from a hybridization event between ancestors of Nicotiana sylvestris and Nicotiana tomentosiformis approximately 200 000 years ago. This resulted in tobacco having a haploid genome size of 4500 million base pairs, approximately four times larger than the related tomato (Solanum lycopersicum) and potato (Solanum tuberosum) genomes. In this study, a physical map containing 9750 contigs of bacterial artificial chromosomes (BACs) was constructed. The mean contig size was 462 kbp, and the calculated genome coverage equaled the estimated tobacco genome size. We used a method for determination of the ancestral origin of the genome by annotation of WGP sequence tags. This assignment agreed with the ancestral annotation available from the tobacco genetic map, and may be used to investigate the evolution of homoeologous genome segments after polyploidization. The map generated is an essential scaffold for the tobacco genome. We propose the combination of WGP physical mapping technology and tag profiling of ancestral lines as a generally applicable method to elucidate the ancestral origin of genome segments of polyploid species. The physical mapping of genes and their origins will enable application of biotechnology to polyploid plants aimed at accelerating and increasing the precision of breeding for abiotic and biotic stress resistance.
doi:10.1111/tpj.12247
PMCID: PMC3824204  PMID: 23672264
physical map; genome; tobacco; Nicotiana tabacum; polyploidy; whole-genome profiling; next-generation sequencing
8.  Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species 
BMC Plant Biology  2007;7:24.
Background
Endogenous pararetroviral sequences (EPRVs) are a recently discovered class of repetitive sequences that is broadly distributed in the plant kingdom. The potential contribution of EPRVs to plant pathogenicity or, conversely, to virus resistance is just beginning to be explored. Some members of the family Solanaceae are particularly rich in EPRVs. In previous work, EPRVs have been characterized molecularly in various species of Nicotiana including N.tabacum (tobacco) and Solanum tuberosum (potato). Here we describe a family of EPRVs in cultivated tomato (Solanum lycopersicum L.) and a wild relative (S.habrochaites).
Results
Molecular cloning and DNA sequence analysis revealed that tomato EPRVs (named LycEPRVs) are most closely related to those in tobacco. The sequence similarity of LycEPRVs in S.lycopersicum and S.habrochaites indicates they are potentially derived from the same pararetrovirus. DNA blot analysis revealed a similar genomic organization in the two species, but also some independent excision or insertion events after species separation, or flanking sequence divergence. LycEPRVs share with the tobacco elements a disrupted genomic structure and frequent association with retrotransposons. Fluorescence in situ hybridization revealed that copies of LycEPRV are dispersed on all chromosomes in predominantly heterochromatic regions. Methylation of LycEPRVs was detected in CHG and asymmetric CHH nucleotide groups. Although normally quiescent EPRVs can be reactivated and produce symptoms of infection in some Nicotiana interspecific hybrids, a similar pathogenicity of LycEPRVs could not be demonstrated in Solanum L. section Lycopersicon [Mill.] hybrids. Even in healthy plants, however, transcripts derived from multiple LycEPRV loci and short RNAs complementary to LycEPRVs were detected and were elevated upon infection with heterologous viruses encoding suppressors of PTGS.
Conclusion
The analysis of LycEPRVs provides further evidence for the extensive invasion of pararetroviral sequences into the genomes of solanaceous plants. The detection of asymmetric CHH methylation and short RNAs, which are hallmarks of RNAi in plants, suggests that LycEPRVs are controlled by an RNA-mediated silencing mechanism.
doi:10.1186/1471-2229-7-24
PMCID: PMC1899175  PMID: 17517142
9.  Comparative BAC end sequence analysis of tomato and potato reveals overrepresentation of specific gene families in potato 
BMC Plant Biology  2008;8:34.
Background
Tomato (Solanum lycopersicon) and potato (S. tuberosum) are two economically important crop species, the genomes of which are currently being sequenced. This study presents a first genome-wide analysis of these two species, based on two large collections of BAC end sequences representing approximately 19% of the tomato genome and 10% of the potato genome.
Results
The tomato genome has a higher repeat content than the potato genome, primarily due to a higher number of retrotransposon insertions in the tomato genome. On the other hand, simple sequence repeats are more abundant in potato than in tomato. The two genomes also differ in the frequency distribution of SSR motifs. Based on EST and protein alignments, potato appears to contain up to 6,400 more putative coding regions than tomato. Major gene families such as cytochrome P450 mono-oxygenases and serine-threonine protein kinases are significantly overrepresented in potato, compared to tomato. Moreover, the P450 superfamily appears to have expanded spectacularly in both species compared to Arabidopsis thaliana, suggesting an expanded network of secondary metabolic pathways in the Solanaceae. Both tomato and potato appear to have a low level of microsynteny with A. thaliana. A higher degree of synteny was observed with Populus trichocarpa, specifically in the region between 15.2 and 19.4 Mb on P. trichocarpa chromosome 10.
Conclusion
The findings in this paper present a first glimpse into the evolution of Solanaceous genomes, both within the family and relative to other plant species. When the complete genome sequences of these species become available, whole-genome comparisons and protein- or repeat-family specific studies may shed more light on the observations made here.
doi:10.1186/1471-2229-8-34
PMCID: PMC2324086  PMID: 18405374
10.  SolRgene: an online database to explore disease resistance genes in tuber-bearing Solanum species 
BMC Plant Biology  2011;11:116.
Background
The cultivated potato (Solanum tuberosum L.) is an important food crop, but highly susceptible to many pathogens. The major threat to potato production is the Irish famine pathogen Phytophthora infestans, which causes the devastating late blight disease. Potato breeding makes use of germplasm from wild relatives (wild germplasm) to introduce resistances into cultivated potato. The Solanum section Petota comprises tuber-bearing species that are potential donors of new disease resistance genes. The aim of this study was to explore Solanum section Petota for resistance genes and generate a widely accessible resource that is useful for studying and implementing disease resistance in potato.
Description
The SolRgene database contains data on resistance to P. infestans and presence of R genes and R gene homologues in Solanum section Petota. We have explored Solanum section Petota for resistance to late blight in high throughput disease tests under various laboratory conditions and in field trials. From resistant wild germplasm, segregating populations were generated and assessed for the presence of resistance genes. All these data have been entered into the SolRgene database. To facilitate genetic and resistance gene evolution studies, phylogenetic data of the entire SolRgene collection are included, as well as a tool for generating phylogenetic trees of selected groups of germplasm. Data from resistance gene allele-mining studies are incorporated, which enables detection of R gene homologs in related germplasm. Using these resources, various resistance genes have been detected and some of these have been cloned, whereas others are in the cloning pipeline. All this information is stored in the online SolRgene database, which allows users to query resistance data, sequences, passport data of the accessions, and phylogenic classifications.
Conclusion
Solanum section Petota forms the basis of the SolRgene database, which contains a collection of resistance data of an unprecedented size and precision. Complemented with R gene sequence data and phylogenetic tools, SolRgene can be considered the primary resource for information on R genes from potato and wild tuber-bearing relatives.
doi:10.1186/1471-2229-11-116
PMCID: PMC3166922  PMID: 21851635
11.  Flower colour and cytochromes P450† 
Cytochromes P450 play important roles in biosynthesis of flavonoids and their coloured class of compounds, anthocyanins, both of which are major floral pigments. The number of hydroxyl groups on the B-ring of anthocyanidins (the chromophores and precursors of anthocyanins) impact the anthocyanin colour, the more the bluer. The hydroxylation pattern is determined by two cytochromes P450, flavonoid 3′-hydroxylase (F3′H) and flavonoid 3′,5′-hydroxylase (F3′5′H) and thus they play a crucial role in the determination of flower colour. F3′H and F3′5′H mostly belong to CYP75B and CYP75A, respectively, except for the F3′5′Hs in Compositae that were derived from gene duplication of CYP75B and neofunctionalization. Roses and carnations lack blue/violet flower colours owing to the deficiency of F3′5′H and therefore lack the B-ring-trihydroxylated anthocyanins based upon delphinidin. Successful redirection of the anthocyanin biosynthesis pathway to delphinidin was achieved by expressing F3′5′H coding regions resulting in carnations and roses with novel blue hues that have been commercialized. Suppression of F3′5′H and F3′H in delphinidin-producing plants reduced the number of hydroxyl groups on the anthocyanidin B-ring resulting in the production of monohydroxylated anthocyanins based on pelargonidin with a shift in flower colour to orange/red. Pelargonidin biosynthesis is enhanced by additional expression of a dihydroflavonol 4-reductase that can use the monohydroxylated dihydrokaempferol (the pelargonidin precursor). Flavone synthase II (FNSII)-catalysing flavone biosynthesis from flavanones is also a P450 (CYP93B) and contributes to flower colour, because flavones act as co-pigments to anthocyanins and can cause blueing and darkening of colour. However, transgenic plants expression of a FNSII gene yielded paler flowers owing to a reduction of anthocyanins because flavanones are precursors of anthocyanins and flavones.
doi:10.1098/rstb.2012.0432
PMCID: PMC3538422  PMID: 23297355
anthocyanin; anthocyanidin; flavonoid; flavonoid 3′-hydroxylase; flavonoid 3′,5′-hydroxylase; flavone synthase
12.  Host Status of Different Potato (Solanum tuberosum) Varieties and Hatching in Root Diffusates of Globodera ellingtonae 
Journal of Nematology  2013;45(3):195-201.
Globodera ellingtonae was detected in Oregon in 2008. In order to make decisions regarding the regulation of this nematode, knowledge of its biology is required. We determined the host status of a diversity of potato (Solanum tuberosum) varieties in soil-based experiments and identified hatching stimulants in in vitro hatching assays. ‘Russet Burbank,’ ‘Desiree,’ ‘Modac,’ ‘Norland,’ ‘Umatilla,’ and ‘Yukon Gold’ were good hosts (RF > 14) for G. ellingtonae. Potato varieties ‘Maris Piper,’ ‘Atlantic,’ and ‘Satina,’ all which contain the Ro1 gene that confers resistance to G. rostochiensis, were not hosts for G. ellingtonae. In in vitro hatching assays, G. ellingtonae hatched readily in the presence of diffusates from potato (PRD) and tomato (Solanum lycopersicum; TRD). Egg hatch occurred in an average of between 87% and 90% of exposed cysts, with an average of between 144 and 164 juveniles emerging per cyst, from PRD- and TRD-treated cysts, respectively. This nematode hatched rapidly in the presence of PRD and TRD, with at least 66% of total hatch occurring by day 3 of exposure. There was no dose-response of egg hatch to concentrations of PRD or TRD ranging from 1:5 to 1:100 diffusate to water. When G. ellingtonae was exposed to root diffusates from 21 different plants, hatch occurred in 0% to 70% of exposed cysts, with an average of between 0 to 27 juveniles emerging per cyst. When root diffusate-exposed cysts were subsequently transferred to PRD to test viability, root diffusates from arugula (Eruca sativa), sudangrass (Sorghum bicolor subsp. drummondii), and common vetch (Vicia sativa) continued to inhibit egg hatch compared with the other root diffusates or water in which hatch occurred readily (60 to 182 juveniles emerging per cyst). Previously known hatching stimulants of G. rostochiensis and G. pallida, sodium metavanadate, sodium orthovanadate, and sodium thiocyanate, stimulated some egg hatch. Although, Globodera ellingtonae hatched readily in PRD and TRD and reproduced on potato, the pathogenicity of this nematode on potato remains to be determined.
PMCID: PMC3792837  PMID: 24115784
behavior; diffusates; Globodera; hatching; potato; resistance; tomato
13.  Constitutively expressed DHAR and MDHAR influence fruit, but not foliar ascorbate levels in tomato 
Plant Physiology and Biochemistry  2011;49(10):1244-1249.
Vitamin C (l-ascorbate, AsA) is an essential nutrient required in key metabolic functions in humans and must be obtained from the diet, mainly from fruits and vegetables. Given its importance in human health and plant physiology we sought to examine the role of the ascorbate recycling enzymes monodehydroascorbate reductase (MDHAR) and dehydroascorbate reductase (DHAR) in tomato (Solanum lycopersicum), an economically important fruit crop. Cytosolic-targeted tomato genes Mdhar and Dhar were cloned and over-expressed under a constitutive promoter in tomato var. Micro-Tom. Lines with increased protein levels and enzymatic activity were identified and examined. Mature green and red ripe fruit from DHAR over-expressing lines had a 1.6 fold increase in AsA content in plants grown under relatively low light conditions (150 µmol m−2 s−1). Conversely, MDHAR over-expressers had significantly reduced AsA levels in mature green fruits by 0.7 fold. Neither over-expressing line had altered levels of AsA in foliar tissues. These results underscore a complex regulation of the AsA pool size in tomato.
doi:10.1016/j.plaphy.2011.08.003
PMCID: PMC3310224  PMID: 21875809
14.  Analysis of 90 Mb of the potato genome reveals conservation of gene structures and order with tomato but divergence in repetitive sequence composition 
BMC Genomics  2008;9:286.
Background
The Solanaceae family contains a number of important crop species including potato (Solanum tuberosum) which is grown for its underground storage organ known as a tuber. Albeit the 4th most important food crop in the world, other than a collection of ~220,000 Expressed Sequence Tags, limited genomic sequence information is currently available for potato and advances in potato yield and nutrition content would be greatly assisted through access to a complete genome sequence. While morphologically diverse, Solanaceae species such as potato, tomato, pepper, and eggplant share not only genes but also gene order thereby permitting highly informative comparative genomic analyses.
Results
In this study, we report on analysis 89.9 Mb of potato genomic sequence representing 10.2% of the genome generated through end sequencing of a potato bacterial artificial chromosome (BAC) clone library (87 Mb) and sequencing of 22 potato BAC clones (2.9 Mb). The GC content of potato is very similar to Solanum lycopersicon (tomato) and other dicotyledonous species yet distinct from the monocotyledonous grass species, Oryza sativa. Parallel analyses of repetitive sequences in potato and tomato revealed substantial differences in their abundance, 34.2% in potato versus 46.3% in tomato, which is consistent with the increased genome size per haploid genome of these two Solanum species. Specific classes and types of repetitive sequences were also differentially represented between these two species including a telomeric-related repetitive sequence, ribosomal DNA, and a number of unclassified repetitive sequences. Comparative analyses between tomato and potato at the gene level revealed a high level of conservation of gene content, genic feature, and gene order although discordances in synteny were observed.
Conclusion
Genomic level analyses of potato and tomato confirm that gene sequence and gene order are conserved between these solanaceous species and that this conservation can be leveraged in genomic applications including cross-species annotation and genome sequencing initiatives. While tomato and potato share genic features, they differ in their repetitive sequence content and composition suggesting that repetitive sequences may have a more significant role in shaping speciation than previously reported.
doi:10.1186/1471-2164-9-286
PMCID: PMC2442093  PMID: 18554403
15.  Organization and Evolution of Subtelomeric Satellite Repeats in the Potato Genome 
G3: Genes|Genomes|Genetics  2011;1(2):85-92.
Subtelomeric domains immediately adjacent to telomeres represent one of the most dynamic and rapidly evolving regions in eukaryotic genomes. A common feature associated with subtelomeric regions in different eukaryotes is the presence of long arrays of tandemly repeated satellite sequences. However, studies on molecular organization and evolution of subtelomeric repeats are rare. We isolated two subtelomeric repeats, CL14 and CL34, from potato (Solanum tuberosum). The CL14 and CL34 repeats are organized as independent long arrays, up to 1-3 Mb, of 182 bp and 339 bp monomers, respectively. The CL14 and CL34 repeat arrays are directly connected with the telomeric repeats at some chromosomal ends. The CL14 repeat was detected at the subtelomeric regions among highly diverged Solanum species, including tomato (Solanum lycopersicum). In contrast, CL34 was only found in potato and its closely related species. Interestingly, the CL34 repeat array was always proximal to the telomeres when both CL14 and CL34 were found at the same chromosomal end. In addition, the CL34 repeat family showed more sequence variability among monomers compared with the CL14 repeat family. We conclude that the CL34 repeat family emerged recently from the subtelomeric regions of potato chromosomes and is rapidly evolving. These results provide further evidence that subtelomeric domains are among the most dynamic regions in eukaryotic genomes.
doi:10.1534/g3.111.000125
PMCID: PMC3276127  PMID: 22384321
16.  High-Throughput Genomics Enhances Tomato Breeding Efficiency 
Current Genomics  2009;10(1):1-9.
Tomato (Solanum lycopersicum) is considered a model plant species for a group of economically important crops, such as potato, pepper, eggplant, since it exhibits a reduced genomic size (950 Mb), a short generation time, and routine transformation technologies. Moreover, it shares with the other Solanaceous plants the same haploid chromosome number and a high level of conserved genomic organization. Finally, many genomic and genetic resources are actually available for tomato, and the sequencing of its genome is in progress. These features make tomato an ideal species for theoretical studies and practical applications in the genomics field. The present review describes how structural genomics assist the selection of new varieties resistant to pathogens that cause damage to this crop. Many molecular markers highly linked to resistance genes and cloned resistance genes are available and could be used for a high-throughput screening of multiresistant varieties. Moreover, a new genomics-assisted breeding approach for improving fruit quality is presented and discussed. It relies on the identification of genetic mechanisms controlling the trait of interest through functional genomics tools. Following this approach, polymorphisms in major gene sequences responsible for variability in the expression of the trait under study are then exploited for tracking simultaneously favourable allele combinations in breeding programs using high-throughput genomic technologies. This aims at pyramiding in the genetic background of commercial cultivars alleles that increase their performances. In conclusion, tomato breeding strategies supported by advanced technologies are expected to target increased productivity and lower costs of improved genotypes even for complex traits.
doi:10.2174/138920209787581226
PMCID: PMC2699839  PMID: 19721805
Solanum lycopersicum; genetic and genomic resources; molecular markers; microarray; resistance to pathogens; fruit quality.
17.  Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations 
The Plant Journal  2013;76(3):530-544.
Summary
RenSeq is a NB-LRR (nucleotide binding-site leucine-rich repeat) gene-targeted, Resistance gene enrichment and sequencing method that enables discovery and annotation of pathogen resistance gene family members in plant genome sequences. We successfully applied RenSeq to the sequenced potato Solanum tuberosum clone DM, and increased the number of identified NB-LRRs from 438 to 755. The majority of these identified R gene loci reside in poorly or previously unannotated regions of the genome. Sequence and positional details on the 12 chromosomes have been established for 704 NB-LRRs and can be accessed through a genome browser that we provide. We compared these NB-LRR genes and the corresponding oligonucleotide baits with the highest sequence similarity and demonstrated that ∼80% sequence identity is sufficient for enrichment. Analysis of the sequenced tomato S. lycopersicum ‘Heinz 1706’ extended the NB-LRR complement to 394 loci. We further describe a methodology that applies RenSeq to rapidly identify molecular markers that co-segregate with a pathogen resistance trait of interest. In two independent segregating populations involving the wild Solanum species S. berthaultii (Rpi-ber2) and S. ruiz-ceballosii (Rpi-rzc1), we were able to apply RenSeq successfully to identify markers that co-segregate with resistance towards the late blight pathogen Phytophthora infestans. These SNP identification workflows were designed as easy-to-adapt Galaxy pipelines.
doi:10.1111/tpj.12307
PMCID: PMC3935411  PMID: 23937694
NB-LRR; pathogen resistance; Solanaceae; target enrichment; next-generation sequencing; Solanum tuberosum Group Phureja clone DM1-3 516 R44; Solanum ruiz-ceballosii; Solanum berthaultii; Solanum lycopersicum; technical advance
18.  Gene-based microsatellite development for mapping and phylogeny studies in eggplant 
BMC Genomics  2008;9:357.
Background
Eggplant (Solanum melongena L.) is a member of the Solanaceae family. In spite of its widespread cultivation and nutritional and economic importance, its genome has not as yet been extensively investigated. Few analyses have been carried out to determine the genetic diversity of eggplant at the DNA level, and linkage relationships have not been well characterised. As for the other Solanaceae crop species (potato, tomato and pepper), the level of intra-specific polymorphism appears to be rather limited, and so it is important that an effort is made to develop more informative DNA markers to make progress in understanding the genetics of eggplant and to advance its breeding. The aim of the present work was to develop a set of functional microsatellite (SSR) markers, via an in silico analysis of publicly available DNA sequence.
Results
From >3,300 genic DNA sequences, 50 SSR-containing candidates suitable for primer design were recovered. Of these, 39 were functional, and were then applied to a panel of 44 accessions, of which 38 were cultivated eggplant varieties, and six were from related Solanum species. The usefulness of the SSR assays for diversity analysis and taxonomic discrimination was demonstrated by constructing a phylogeny based on SSR polymorphisms, and by the demonstration that most were also functional when tested with template from tomato, pepper and potato. As a results of BLASTN analyses, several eggplant SSRs were found to have homologous counterparts in the phylogenetically related species, which carry microsatellite motifs in the same position.
Conclusion
The set of eggplant EST-SSR markers was informative for phylogenetic analysis and genetic mapping. Since EST-SSRs lie within expressed sequence, they have the potential to serve as perfect markers for genes determining variation in phenotype. Their high level of transferability to other Solanaceae species can be used to provide anchoring points for the integration of genetic maps across species.
doi:10.1186/1471-2164-9-357
PMCID: PMC2527019  PMID: 18667065
19.  Effector Genomics Accelerates Discovery and Functional Profiling of Potato Disease Resistance and Phytophthora Infestans Avirulence Genes 
PLoS ONE  2008;3(8):e2875.
Potato is the world's fourth largest food crop yet it continues to endure late blight, a devastating disease caused by the Irish famine pathogen Phytophthora infestans. Breeding broad-spectrum disease resistance (R) genes into potato (Solanum tuberosum) is the best strategy for genetically managing late blight but current approaches are slow and inefficient. We used a repertoire of effector genes predicted computationally from the P. infestans genome to accelerate the identification, functional characterization, and cloning of potentially broad-spectrum R genes. An initial set of 54 effectors containing a signal peptide and a RXLR motif was profiled for activation of innate immunity (avirulence or Avr activity) on wild Solanum species and tentative Avr candidates were identified. The RXLR effector family IpiO induced hypersensitive responses (HR) in S. stoloniferum, S. papita and the more distantly related S. bulbocastanum, the source of the R gene Rpi-blb1. Genetic studies with S. stoloniferum showed cosegregation of resistance to P. infestans and response to IpiO. Transient co-expression of IpiO with Rpi-blb1 in a heterologous Nicotiana benthamiana system identified IpiO as Avr-blb1. A candidate gene approach led to the rapid cloning of S. stoloniferum Rpi-sto1 and S. papita Rpi-pta1, which are functionally equivalent to Rpi-blb1. Our findings indicate that effector genomics enables discovery and functional profiling of late blight R genes and Avr genes at an unprecedented rate and promises to accelerate the engineering of late blight resistant potato varieties.
doi:10.1371/journal.pone.0002875
PMCID: PMC2483939  PMID: 18682852
20.  Genetic and genomic approaches for R-gene mediated disease resistance in tomato: retrospects and prospects 
Plant Cell Reports  2012;31(6):973-985.
Tomato (Solanum lycopersicum) is one of the world’s most important vegetable crops. Managing the health of this crop can be particularly challenging; crop resistance may be overcome by new pathogen races while new pathogens have been introduced by global agricultural markets. Tomato is extensively used as a model plant for resistance studies and much has been attained through both genetic and biotechnological approaches. In this paper, we illustrate genomic methods currently employed to preserve resistant germplasm and to facilitate the study and transfer of resistance genes, and we describe the genomic organization of R-genes. Patterns of gene activation during disease resistance response, identified through functional approaches, are depicted. We also describe the opportunities offered by the use of new genomic technologies, including high-throughput DNA sequencing, large-scale expression data production and the comparative hybridization technique, whilst reporting multifaceted approaches to achieve genetic tomato disease control. Future strategies combining the huge amount of genomic and genetic data will be able to accelerate development of novel resistance varieties sustainably on a worldwide basis. Such strategies are discussed in the context of the latest insights obtained in this field.
doi:10.1007/s00299-012-1234-z
PMCID: PMC3351601  PMID: 22350316
Solanum lycopersicum; Disease resistance; Genomic tools; Emerging technologies; New breeding methods
21.  Genomics of Fungal Disease Resistance in Tomato 
Current Genomics  2010;11(1):30-39.
Tomato (Solanum lycopersicum) is an important vegetable crop worldwide. Often times, its production is hindered by fungal diseases. Important fungal diseases limiting tomato production are late blight, caused by Phytophthora infestans, early blight, caused by Alternaria solanii, and septoria leaf spot, caused by Septoria lycopersici, fusarium wilt caused by Fusarium oxysporium fsp. oxysporium, and verticilium wilt caused by Verticilium dahlea. The Phytophthora infestans is the same fungus that caused the devastating loss of potato in Europe in 1845. A similar magnitude of crop loss in tomato has not occurred but Phytophthora infestans has caused the complete loss of tomato crops around the world on a small scale. Several attempts have been made through conventional breeding and the molecular biological approaches to understand the biology of host-pathogen interaction so that the disease can be managed and crop loss prevented. In this review, we present a comprehensive analysis of information produced by molecular genetic and genomic experiments on host-pathogen interactions of late blight, early blight, septoria leaf spot, verticilim wilt and fusarium wilt in tomato. Furthermore, approaches adopted to manage these diseases in tomato including genetic transformation are presented. Attempts made to link molecular markers with putative genes and their use in crop improvement are discussed.
doi:10.2174/138920210790217927
PMCID: PMC2851114  PMID: 20808521
Comparative genomics; functional genomics; genomics; QTL analysis; Solanum lycopersicum; tomato.
22.  Oligonucleotide array discovery of polymorphisms in cultivated tomato (Solanum lycopersicum L.) reveals patterns of SNP variation associated with breeding 
BMC Genomics  2009;10:466.
Background
Cultivated tomato (Solanum lycopersicum L.) has narrow genetic diversity that makes it difficult to identify polymorphisms between elite germplasm. We explored array-based single feature polymorphism (SFP) discovery as a high-throughput approach for marker development in cultivated tomato.
Results
Three varieties, FL7600 (fresh-market), OH9242 (processing), and PI114490 (cherry) were used as a source of genomic DNA for hybridization to oligonucleotide arrays. Identification of SFPs was based on outlier detection using regression analysis of normalized hybridization data within a probe set for each gene. A subset of 189 putative SFPs was sequenced for validation. The rate of validation depended on the desired level of significance (α) used to define the confidence interval (CI), and ranged from 76% for polymorphisms identified at α ≤ 10-6 to 60% for those identified at α ≤ 10-2. Validation percentage reached a plateau between α ≤ 10-4 and α ≤ 10-7, but failure to identify known SFPs (Type II error) increased dramatically at α ≤ 10-6. Trough sequence validation, we identified 279 SNPs and 27 InDels in 111 loci. Sixty loci contained ≥ 2 SNPs per locus. We used a subset of validated SNPs for genetic diversity analysis of 92 tomato varieties and accessions. Pairwise estimation of θ (Fst) suggested significant differentiation between collections of fresh-market, processing, vintage, Latin American (landrace), and S. pimpinellifolium accessions. The fresh-market and processing groups displayed high genetic diversity relative to vintage and landrace groups. Furthermore, the patterns of SNP variation indicated that domestication and early breeding practices have led to progressive genetic bottlenecks while modern breeding practices have reintroduced genetic variation into the crop from wild species. Finally, we examined the ratio of non-synonymous (Ka) to synonymous substitutions (Ks) for 20 loci with multiple SNPs (≥ 4 per locus). Six of 20 loci showed ratios of Ka/Ks ≥ 0.9.
Conclusion
Array-based SFP discovery was an efficient method to identify a large number of molecular markers for genetics and breeding in elite tomato germplasm. Patterns of sequence variation across five major tomato groups provided insight into to the effect of human selection on genetic variation.
doi:10.1186/1471-2164-10-466
PMCID: PMC2763011  PMID: 19818135
23.  Comparative genome analysis of Solanum lycopersicum and Solanum tuberosum 
Bioinformation  2013;9(18):923-928.
Solanum lycopersicum and Solanum tuberosum are agriculturally important crop species as they are rich sources of starch, protein, antioxidants, lycopene, beta-carotene, vitamin C, and fiber. The genomes of S. lycopersicum and S. tuberosum are currently available. However the linear strings of nucleotides that together comprise a genome sequence are of limited significance by themselves. Computational and bioinformatics approaches can be used to exploit the genomes for fundamental research for improving their varieties. The comparative genome analysis, Pfam analysis of predicted reviewed paralogous proteins was performed. It was found that S. lycopersicum proteins belong to more families, domains and clans in comparison with S. tuberosum. It was also found that mostly intergenic regions are conserved in two genomes followed by exons, intron and UTR. This can be exploited to predict regions between genomes that are similar to each other and to study the evolutionary relationship between two genomes, leading towards the development of disease resistance, stress tolerance and improved varieties of tomato.
doi:10.6026/97320630009923
PMCID: PMC3842579  PMID: 24307771
S. lycopersicum; S. tuberosum; genome
24.  Glycosyltransferase efficiently controls phenylpropanoid pathway 
BMC Biotechnology  2008;8:25.
Background
In a previous study, anthocyanin levels in potato plants were increased by manipulating genes connected with the flavonoid biosynthesis pathway. However, starch content and tuber yield were dramatically reduced in the transgenic plants, which over-expressed dihydroflavonol reductase (DFR).
Results
Transgenic plants over-expressing dihydroflavonol reductase (DFR) were subsequently transformed with the cDNA coding for the glycosyltransferase (UGT) of Solanum sogarandinum in order to obtain plants with a high anthocyanin content without reducing tuber yield and quality. Based on enzyme studies, the recombinant UGT is a 7-O-glycosyltransferase whose natural substrates include both anthocyanidins and flavonols such as kaempferol and quercetin. In the super-transformed plants, tuber production was much higher than in the original transgenic plants bearing only the transgene coding for DFR, and was almost the same as in the control plants. The anthocyanin level was lower than in the initial plants, but still higher than in the control plants. Unexpectedly, the super-transformed plants also produced large amounts of kaempferol, chlorogenic acid, isochlorogenic acid, sinapic acid and proanthocyanins.
Conclusion
In plants over-expressing both the transgene for DFR and the transgene for UGT, the synthesis of phenolic acids was diverted away from the anthocyanin branch. This represents a novel approach to manipulating phenolic acids synthesis in plants.
doi:10.1186/1472-6750-8-25
PMCID: PMC2294120  PMID: 18321380
25.  Variation Revealed by SNP Genotyping and Morphology Provides Insight into the Origin of the Tomato 
PLoS ONE  2012;7(10):e48198.
Tomato, Solanum lycopersicum, is divided into two widely distributed varieties: the cultivated S. lycopersicum var. lycopersicum, and the weedy S. lycopersicum var. cerasiforme. Solanum pimpinellifolium is the most closely related wild species of tomato.
The roles of S. pimpinellifolium and S. l. cerasiforme during the domestication of tomato are still under debate. Some authors consider S. l. cerasiforme to be the ancestor, whereas others think that S. l. cerasiforme is an admixture of S. pimpinellifolium and the cultivated S. l. lycopersicum. It is also not clear whether the domestication occurred in the Andean region or in Mesoamerica. We characterized 272 accessions (63 S. pimpinellifolium, 106 S. l. cerasiforme, 95 S. l. lycopersicum and 8 derived from hybridization processes) were morphologically and genetically using the SolCap platform (7,414 SNPs). The two species were distinguished in a PCA analysis and displayed a rich geographic structure. Solanum lycopersicum var. cerasiforme and S. l. lycopersicum were also differentiated in the PCA and Structure analyses, which supports maintaining them as different varieties. Solanum pimpinellifolium and the Andean S. l. cerasiforme were more diverse than the non-Andean S. lycopersicum. Solanum lycopersicum var. cerasiforme was morphologically and molecularly intermediate between S. pimpinellifolium and tomato. Solanum lycopersicum var. cerasiforme, with the exception of several Ecuadorian and Mexican accessions, is composed of the products of admixture processes according to the Structure analysis. The non-admixtured S. l. cerasiforme might be similar to the ancestral cultivars from which the cultivated tomato originated, and presents remarkable morphological diversity, including fruits of up to 6 cm in diameter. The data obtained would fit a model in which a pre-domestication took place in the Andean region, with the domestication being completed in Mesoamerica. Subsequently, the Spaniards took plants from Mesoamerica to Spain and from there they were exported to the rest of the world.
doi:10.1371/journal.pone.0048198
PMCID: PMC3485194  PMID: 23118951

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