A DArT marker-based linkage map for wild potato Solanum bulbocastanum facilitates structural comparisons between SolanumA and B genomes
© Iorizzo et al.; licensee BioMed Central Ltd. 2014
Received: 16 May 2014
Accepted: 29 October 2014
Published: 18 November 2014
Wild potato Solanum bulbocastanum is a rich source of genetic resistance against a variety of pathogens. It belongs to a taxonomic group of wild potato species sexually isolated from cultivated potato. Consistent with genetic isolation, previous studies suggested that the genome of S. bulbocastanum (B genome) is structurally distinct from that of cultivated potato (A genome). However, the genome architecture of the species remains largely uncharacterized. The current study employed Diversity Arrays Technology (DArT) to generate a linkage map for S. bulbocastanum and compare its genome architecture with those of potato and tomato.
Two S. bulbocastanum parental linkage maps comprising 458 and 138 DArT markers were constructed. The integrated map comprises 401 non-redundant markers distributed across 12 linkage groups for a total length of 645 cM. Sequencing and alignment of DArT clones to reference physical maps from tomato and cultivated potato allowed direct comparison of marker orders between species. A total of nine genomic segments informative in comparative genomic studies were identified. Seven genome rearrangements correspond to previously-reported structural changes that have occurred since the speciation of tomato and potato. We also identified two S. bulbocastanum genomic regions that differ from cultivated potato, suggesting possible chromosome divergence between Solanum A and B genomes.
The linkage map developed here is the first medium density map of S. bulbocastanum and will assist mapping of agronomical genes and QTLs. The structural comparison with potato and tomato physical maps is the first genome wide comparison between Solanum A and B genomes and establishes a foundation for further investigation of B genome-specific structural chromosome rearrangements.
The genus Solanum includes agronomically important plants such as potato (S. tuberosum), tomato (S. lycopersicum) and eggplant (S. melongena). Although distinct in terms of morphology and culinary utility, molecular dating suggests that potato and tomato are closely related species, having diverged from a common ancestor 7.3 million years ago . Today, the potato clade comprises approximately 200 tuber-bearing Solanum species, including the cultivated potato and wild relatives native to South, Central, and North America. These wild species are potentially rich sources of genes for the improvement of the cultivated potato.
As a tool for the utilization of wild crop relatives to improve cultivated species, Harlan and Wet  developed the Gene Pool Concept with the primary, secondary, and tertiary gene pools reflecting crossability of wild species with cultivated crop plants. Because they are sexually compatible with cultivated species, germplasm in the primary and secondary gene pools can be directly utilized for crop improvement. In contrast, tertiary gene pool species are sexually isolated from cultivated crops and the genes they harbor cannot be accessed using traditional breeding approaches. Among potato species, the Endosperm Balance Number  predicts the crossability of species, with the cultivated potato assigned an EBN4 and most secondary gene pool species assigned to EBN2. Manipulation of potato ploidy levels can enable cross compatibility between secondary genepool, EBN2 species and the EBN4 cultivated potato, allowing incorporation of genes from wild species for crop improvement. In contrast, about 20 wild potato species are sexually isolated from cultivated potato and comprise the tertiary gene pool for S. tuberosum. These species predominantly have an EBN1 and post-zygotic barriers have significantly precluded widespread use of EBN1 species in potato breeding.
Among EBN1 potato species, the diploid (2n = 2x = 24) S. bulbocastanum, a native of southern Mexico and Guatemala, has long been of interest to potato breeders. The species is a famous source of resistance to late blight disease - and is a documented source of nematode resistance . Like other tertiary gene pool species, however, S. bulbocastanum is sexually isolated from cultivated potato ,. Although costly and time consuming, late blight resistance genes have been transferred from S. bulbocastanum to the cultivated potato genome using multi-species bridge crossing, somatic hybridization, and transgenic techniques -. Morphologically, S. bulbocastanum is one of the most distinct tuber-bearing potato species  and both morphology and molecular data indicate that S. bulbocastanum is phylogenetically distinct from cultivated potato ,. Consistent with sexual incompatibility and phylogenetic uniqueness, cytological observations have led to conclusions that the genome of S. bulbocastanum (B genome) is structurally distinct from that of cultivated potato (A genome) and those of many other wild potato relatives (A, C, D and P genomes) ,.
Overview of chromosomal rearrangements between the potato and tomato genomes based on comparative cytological and genetic mapping
2 L inversion
a, c, d, e, f
a, c, d, f
10 L inversion
a, c, d, f
a, c, f
a, c, f
Diversity Array Technology (DArT, http://www.diversityarrays.com) is a community-based molecular marker technology that allows high-throughput and cost-effective genotyping of target species, without relying on prior genome sequence information. DArT involves the preparation of an array of individualized clones from a genomic representation, generated from amplified restriction fragments ,. The technology has been successfully utilized in various species including Arabidopsis , wheat , barley , and potatoes ,.
Sliwka et al.  utilized DArT technology to genotype a mapping population of Solanum x michoacanum to map the late blight resistance gene Rpi-mch1. The study generated a linkage map consisting of 798 DArT markers. In a separate study, Sliwka et al.  mapped a second late blight resistance gene Rpi-rzc1 (derived from Solanum ruiz-ceballosii) to chromosome 10 using DArT markers and sequence specific PCR markers. Our group pioneered the development of a DArT platform for genotyping EBN1 tertiary genepool potato species, including S. bulbocastanum . In this study, we employed this DArT array to develop a linkage map for S. bulbocastanum. The generation of medium density genome-wide linkage maps for this species, sequencing of mapped DArT probes, and alignment of DArT sequences to reference sequences  allowed us to compare genome structures between the B genome wild potato and the genomes of cultivated potato and tomato genomes ,.
Results and discussion
Linkage map generation
Solanum bulbocastanum is a highly heterozygous diploid species with up to four alleles per marker locus segregating in an F1 population. This precludes traditional mapping strategies. Instead, we applied the pseudo-testcross strategy , generating two parental linkage maps (one for parent PT29 and one for parent G15) and one integrated linkage map.
Summary of the S. bulbocastanum linkage maps including parental maps (PT29 and G15) and the consensus map
# unique 1
# markers 2
12 + 2
12 + 2
40.2 + 11.8
21 + 3
21 + 3
40.7 + 12.7
2 + 3
2 + 3
1.2 + 8.8
4 + 3 + 2
4 + 3 + 2
17.7 + 39.1 + 9.1
6 + 6
6 + 6
22.3 + 42.7
10 + 7
10 + 7
29.2 + 49.5
4 + 6
4 + 3
20.6 + 8.2
For mapping parent G15, a total of 138 DArT markers were integrated into a linkage map comprising 20 LGs, substantially exceeding the expected 12 LGs (Table 2, Additional file 2: Figure S2). The G15 linkage map covers a genetic distance of 529 cM. Three markers mapped to an identical location (at 0.0 cM) resulting in 135 (98%) uniquely positioned markers with 0.27 markers per cM. The comparatively small number of markers integrated into the G15 map (compared to the PT29 map) is likely due to the fact that PT29, but not G15, was a prominent contributor of features on the potato DArT array. Out of 138 markers incorporated into the G15 parental linkage map, 90 (65%) markers aligned to a unique location on the potato and tomato reference genome sequences, allowing anchorage of all 20 LGs to corresponding chromosomes.
The integrated S. bulbocastanum linkage map comprises 12 LGs with a total of 631 markers, 401 of which are uniquely positioned (64%) (Table 2, Additional file 3: Figure S3). The integrated map spans a total genetic distance of 644.9 cM, averaging 0.62 unique loci per cM. The LG corresponding to potato chromosome 4 is the largest, comprising 103 DArT markers spanning 83.7 cM. To map root-knot nematode resistance (Rmc1) from S. bulbocastanum, Brown et al.  developed a restriction fragment length polymorphism (RFLP) S. bulbocastanum linkage map using a mapping population derived from somatic hybrids between the wild species and cultivated tetraploid potato. A S. bulbocastanum linkage map comprising 48 RFLP markers (belonging to 12 linkage groups) was generated and the locus Rmc1 was mapped. Several linkage maps using a wide range of molecular markers have been developed for S. tuberosum and others relative species . The integrated S. bulbocastanum DArT marker map developed in the current study represents a greater than 10-fold increase in marker density compared to the only previously available genetic map for S. bulbocastanum .
Comparative analysis between the S. bulbocastanumgenetic map and the potato and tomato physical maps
Early comparison of low resolution RFLP linkage maps revealed general conservation of marker order along nine of the 12 chromosomes of potato and tomato with three chromosomes displaying intra-chromosomal, paracentric inversions that structurally distinguished the two genomes . Subsequent increases in marker density and refinement of linkage maps confirmed and expanded these early observations , and sequencing of the potato  and tomato  genomes allowed direct comparisons. In total, sequence analysis identified nine large inversions and numerous small scale inversions that structurally differentiate the potato and tomato genomes . These changes in chromosome structure have accumulated since divergence of the potato and tomato lineages from a common ancestor approximately 7.3 million years ago .
Over that same period of time, the potato clade has diversified to encompass approximately 200 extant tuber bearing Solanum species. Numerous factors including physical separation and sexual isolation due to differences in ploidy and EBN have facilitated morphological and phylogenetic diversification amongst potato species. Solanum bulbocastanum, the focus of the current study, is a diploid, EBN1 species that belongs to the tertiary gene pool for cultivated potato. The species is morphologically distinct, with simple, undivided leaves, and a star-shaped or stellate flower, a morphological characteristic considered to be evolutionarily primitive . In contrast, the cultivated potato is an autotetraploid, 4EBN species with divided leaves and a fused or rotate corolla. Consistent with morphological classification, molecular data support clear phylogenetic distinction between EBN1 species, including S. bulbocastanum, and the cultivated potato .
Classical cytogenetics approaches led to postulations of structurally distinct genome configurations amongst potato species ,-. Various models and terminology were standardized by Matsubayashi . Cultivated potato was designated as an A genome species and S. bulbocastanum was designated as a B genome species. Crosses between cultivated potato and S. bulbocastaum have consistently produced no viable progeny , precluding direct cytological observation of chromosome pairing behaviors between these species. Differences in A and B genome structures, where directly observable, include visible loops in paired chromosomes during pachytene. Hermsen and Ramanna  observed loops during pachytene in F1 progeny resulting from a cross between the A1 genome S. verrucosum and B genome S. bulbocastanum, concluding that the two genomes are structurally distinct, with differentiation consisting of a series of small scale structural differences. Phylogenies constructed based on DNA sequence of nitrate reductase  and Waxy  genes support differentiation of A and B genome species. Importantly, in allopolyploids comprising A and B genomes, these gene sequences remain distinct . To date, no direct molecular comparison of potato A- and B-genome structures has been reported.
Summary of chromosomal rearrangements detected between S. bulbocastanum linkage map and the potato and tomato genomes
LG/chromosome ( S. bulbocastanum )
Position in tomato genome (Mb)
BAC FISH 3
15.4 - 31.9
2 L inversion
43.8 - 47.9
43.9 - 47.5
1.8 - 7.7
0.5 - 5.1
0.4 - 5.0
1.9 - 2.2
1.9 - 2.4
1.1 - 2.5
0.8 - 5.1
0.7 - 6.1
4.2 - 5.1
0.1 - 5.2
0.5 - 3.9
0.2 - 2.8
Seven of the 9 rearrangements represent genome structure changes that have occurred since the initial speciation of the tomato and potato lineages as verified by cytological assays -. These rearrangements involve the long arm of chromosome 2(2 L) and the short arms of chromosome 5(5S), 6(6S), 9(9S), 11(11S) and 12(12S). In each instance, S. bulbocastanum shows high collinearity to the potato genome and rearrangement relative to the tomato genome. For example, a region of the S. bulbocastanum integrated map on LG3 spanning positions 11.6 to 12.2 cM is collinear with potato chr3S but rearranged relative to tomato chr3S. Specifically, DArT markers mapped in this region in S. bulbocastanum align to two disparate tomato chr3 positions: 1.8 Mb and 7.7 Mb (Table 3). Recently Sharma et al.  reported that this tomato 3S region contains an insertion that aligns to potato 3 L. The authors concluded that a translocation across the centromere differentiated potato and tomato chromosome 3. Our results are in agreement. Four markers covering the potato-tomato inversion on chromosome 10 (10 L) co-localized in S. bulbocastanum LG10 at position 12.8 cM. The lack of recombination between the four markers in our S. bulbocastanum F1 population precludes examination of the presence or absence of this rearrangement in the B genome (data not shown).
Collectively, our results suggest that B genome wild potato species share higher collinearity with cultivated potato than tomato, consistent with closer phylogenetic relationships between S. bulbocastanum and cultivated potato than between S. bulbocastanum and tomato .
Importantly, our study also suggests two rearrangements that differentiate S. bulbocastanum from both potato and tomato (Table 3). These comprise two independent inversions on S. bulbocastanum chromosome 2S and 8S (Figure 1). These segments span small genetic and physical distances (around 5-10 cM) and are located near telomere positions. Because these putative rearrangements are signified by relatively few markers, we cannot rule out errors in linkage mapping and greater marker saturation, expanded mapping populations, and other means of further validation by cytogenetic experiments are warranted. Given the phylogenetic distinction of S. bulbocastanum and potato, and cytological observations implying genomic structural differences between these species, we conclude accumulation of chromosomal structural variation in S. bulbocastanum relative to potato is not improbable.
To date no comparative mapping study has explicitly compared Solanum A- and B-genome species. The putative chromosome inversions we observed on S. bulbocastanum chromosomes 2(2S) and 8(S) could comprise a set of genomic structural changes discriminating between the Solanum A- and B-genomes. Expansion of mapping efforts, cytological study or whole genome sequencing of S. bulbocastanum and other B-genome Solanum species may confirm the legitimacy of these regions and may reveal other B-genome specific genomic segments. Since the original A vs. B genome hypotheses are based on low resolution cytological observations , we expected medium density linkage mapping in S. bulbocastanum to offer sufficient resolution to identify structural variations. Our approach demonstrates that molecular mapping with DArT markers followed by genomics analysis of mapped loci enabled identification of large-scale changes in chromosome structure, identifying seven major rearrangements that occurred since potato and tomato diverged.
Owing to their phylogenetic novelty, EBN1, B-genome Solanum species are likely sources of novel disease resistance and agronomic traits . Documentation of predominant collinearity between A and B genome potato species and the validation of the DArT marker platform for comparative analyses provide new opportunities for potato improvement. The sequence of markers CT182, linked to Rmc1 locus  was used to identify the approximate location of this locus in the DArT map. A DarT markers (ID 473601) mapped at 13.3 cM of LG11, localized at position 2.38 Mb of potato Ch11, only 0.2 Mb apart from marker CT182 (2.40 Mb)(Figure 1). This paves the way for rapid mapping of genes underlying traits of interest and comparative approaches to gene mapping and cloning. Our ongoing efforts to isolate and map candidate disease resistance genes in S. bulbocastanum and other B-genome species , are likely to further this potential. Useful genes isolated from B-genome species can be transferred to potato as transgenes . Somatic hybridization  and multi-species bridge crosses  provide non-transgenic approaches to introgress genes from B-genome species into cultivated potato. In these instances, marker aided selection (MAS) may provide a rapid and efficient means of generating improved commercially acceptable potato cultivars. The current study documents that the DArT marker platform could be useful for MAS approaches involving wild species germplasm.
The first medium-density genome-wide linkage map for wild potato S. bulbocastanum was generated, demonstrating the utility of the DArT platform for genotyping wild potato species. Over 600 markers were integrated into the linkage maps, representing a greater than ten-fold increase in marker density compared to previously existing maps for the wild potato species. Sequencing and alignment of DArT clones to reference potato and tomato physical maps allowed a comparison of genetic and physical orders of the markers. Our results indicate that a majority of the markers are collinear between genetic and physical maps. Marker orders on S. bulbocastanum LGs show higher collinearity to the reference potato physical map than to the tomato physical map. Our research will assist comparative mapping of agronomical important genes or QTLs.
Plant material, DNA isolation, and DArT genotyping
Full-sib progeny seeds from a cross between wild potato Solanum bulbocastanum genotypes PT29 and G15 were planted at the University of Minnesota Plant Growth Facilities greenhouse (St. Paul, MN). Leaf tissue from seven week old plants was collected, frozen immediately in liquid nitrogen, and stored at -80°C for DNA extraction using a modified CTAB method .
In collaboration with the Diversity Arrays Technology, Pty. Ltd., a DArT array for wild potatoes (http://www.diversityarrays.com/) comprising over 20,000 features was constructed ,. DNA samples from 92 F1 progeny of the cross PT29 X G15 together with the two parental lines (PT29 and G15) were genotyped using the DArT array and previously established protocols -.
Linkage map construction
We employed the pseudo-testcross strategy  to construct linkage maps. A total of 854 markers were coded into three marker classes. Markers that were heterozygous in PT29 but homozygous in G15 were coded into the lmxll class (490 markers). Markers that were homozygous in PT29 but heterozygous in G15 were coded into the nnxnp class (166 markers). Markers that were heterozygous in both parents were coded as hkxhk markers (198 markers).
Two parental maps were generated using lmxll (PT29 parental map) and nnxp (G15 parental map) markers, respectively. The regression mapping algorithm of JoinMap 4.1 (http://www.kyazma.nl/index.php/mc.JoinMap/) was used to generate the respective parental maps. Kosambi’s mapping function was used in calculating map distances. The two resulting parental maps were then merged into a composite map using anchor markers (hkxhk). Integrated map marker order was largely based on fixed marker orders from parental maps. In cases in which the two parental fixed marker orders could not be simultaneously satisfied, the marker order from PT29 was adopted.
Comparison of marker order with potato and tomato physical maps
DArT clones polymorphic between the S. bulbocastanum mapping parents were subsequently sequenced  and the sequences were aligned to both potato and tomato genome sequences using GenomeThreader  with 70% minimal nucleotide coverage and sequence identity. Only uniquely aligned DArT clones (i.e., DArT sequences anchored to a single location in the reference genome sequence or to a cluster of identical sequences occupying a single contiguous location on the reference genome sequence) were used to compare physical and genetic maps. The comparative alignment information was summarized using a custom Perl script and visualized using MapChart v2.0 . The list of markers, their location in the integrated map, the potato and tomato genomes was provided in Additional file 6.
Availability of supporting data
The data set supporting the results of this article is included in Additional file 7 and available in the Genomic Survey Sequences (GSS) database under accession number KG961889 - KG963311.
Massimo Iorizzo and Liangliang Gao are co-first authors.
We gratefully acknowledge the University of Naples Federico II, for funding the C.A.R.I.N.A. project as part of the collaboration between M.I. and the authors from the Department of Agricultural Sciences, Portici. This research was also funded by USDA-NIFA through the AFRI Competitive Grants Program. Part of this work was funded by the Italian Ministry of University and Research (MiUR)- PON02 R&C 2007-2013 PON02_00395_3215002 GenHORT (D.D. n. 813/Ric.). Computing resources from the Minnesota Supercomputing Institute at the University of Minnesota are greatly appreciated.
- Wu F, Tanksley SD: Chromosomal evolution in the plant family Solanaceae. BMC Genomics. 2010, 11: 182-10.1186/1471-2164-11-182.PubMedPubMed CentralView ArticleGoogle Scholar
- Harlan JR, Wet JMJ: Toward a Rational Classification of Cultivated Plants. Taxon. 1971, 20 (4): 509-517. 10.2307/1218252.View ArticleGoogle Scholar
- Johnston SA, den Nijs TM, Peloquin SJ, Hanneman RE: The significance of genic balance to endosperm development in interspecific crosses. Theor Appl Genet. 1980, 57 (1): 5-9. 10.1007/BF00276002.PubMedView ArticleGoogle Scholar
- Graham KM, Niederhauser JS, Servin L: Studies on fertility and late blight resistance in Solanum bulbocastanum Dun. in Mexico. Can J Bot. 1959, 37 (1): 41-49. 10.1139/b59-003.View ArticleGoogle Scholar
- Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, Haberlach GT, Liu J, Kuang H, Austin-Phillips S, Buell CR, Helgeson JP, Jiang J: Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance against potato late blight pathogen Phytophthora infestans . Proc Natl Acad Sci U S A. 2003, 100 (16): 9128-9133. 10.1073/pnas.1533501100.PubMedPubMed CentralView ArticleGoogle Scholar
- Evd V, Sikkema A, Hekkert BTL, Gros J, Stevens P, Muskens M, Wouters D, Pereira A, Stiekema W, Allefs S: An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 2003, 36 (6): 867-882. 10.1046/j.1365-313X.2003.01934.x.View ArticleGoogle Scholar
- Park TH, Gros J, Sikkema A, Vleeshouwers VGAA, Muskens M, Allefs S, Jacobsen E, Visser RGF, Vossen EAG: The late blight resistance locus Rpi-blb3 from Solanum bulbocastanum belongs to a major late blight R gene cluster on chromosome 4 of potato. Mol Plant Microb Interact. 2005, 18 (7): 722-729. 10.1094/MPMI-18-0722.View ArticleGoogle Scholar
- Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S: The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J. 2005, 44 (2): 208-222. 10.1111/j.1365-313X.2005.02527.x.PubMedView ArticleGoogle Scholar
- Oosumi T, Rockhold DR, Maccree MM, Deahl KL, McCue KF, Belknap WR: Gene Rpi-bt1 from Solanum bulbocastanum confers resistance to late blight in transgenic potatoes. Am J Pot Res. 2009, 86 (6): 456-465. 10.1007/s12230-009-9100-4.View ArticleGoogle Scholar
- Brown CR, Yang CP, Mojtahedi H, Santo GS, Masuelli R: RFLP analysis of resistance to Columbia root-knot nematode derived from Solanum bulbocastanum in a BC2 population. Theor Appl Genet. 1996, 92 (5): 572-576. 10.1007/BF00224560.PubMedView ArticleGoogle Scholar
- Jackson SA, Hanneman RE: Crossability between cultivated and wild tuber- and non-tuber-bearing Solanums . Euphytica. 1999, 109 (1): 51-67. 10.1023/A:1003710817938.View ArticleGoogle Scholar
- Hermsen JGT, Ramanna MS: Double-bridge hybrids of Solanum bulbocastanum and cultivars of Solanum tuberosum . Euphytica. 1973, 22 (3): 457-466. 10.1007/BF00036641.View ArticleGoogle Scholar
- Austin S, Pohlman JD, Brown CR, Mojtahedi H, Santo GS, Douches DS, Helgeson JP: Interspecific somatic hybridization between Solanum tuberosum L. and S. bulbocastanum Dun. as a means of transferring nematode resistance. Am Potato J. 1993, 70 (6): 485-495. 10.1007/BF02849067.View ArticleGoogle Scholar
- Helgeson JP, Pohlman JD, Austin S, Haberlach GT, Wielgus SM, Ronis D, Zambolim L, Tooley P, McGrath JM, James RV: Somatic hybrids between Solanum bulbocastanum and potato: a new source of resistance to late blight. Theor Appl Genet. 1998, 96 (6-7): 738-742. 10.1007/s001220050796.View ArticleGoogle Scholar
- Iovene M, Aversano R, Savarese S, Caruso I, Di Mattero A, Cardi T, Frusciante L, Carputo D: Interspecific somatic hybrids between Solanum bulbocastanum and S. tuberosum and their haploidization for potato breeding. Biol Palntarum. 2012, 56 (1): 1-8. 10.1007/s10535-012-0008-3.View ArticleGoogle Scholar
- Naess SK, Bradeen JM, Wielgus SM, Haberlach GT, McGrath JM, Helgeson JP: Analysis of the introgression of Solanum bulbocastanum DNA into potato breeding lines. Mol Genet Genomics. 2001, 265 (4): 694-704. 10.1007/s004380100465.PubMedView ArticleGoogle Scholar
- Bradeen JM, Iorizzo M, Mollov DS, Raasch J, Kramer LC, Millett BP, Austin-Phillips S, Jiang JM, Carputo D: Higher Copy Numbers of the Potato RB Transgene Correspond to Enhanced Transcript and Late Blight Resistance Levels. Mol Plant Microb Interact. 2009, 22 (4): 437-446. 10.1094/MPMI-22-4-0437.View ArticleGoogle Scholar
- Rodriguez A, Spooner DM: Subspecies boundaries of the wild potatoes Solanum bulbocastanum and S. cardiophyllum based on morphological and nuclear RFLP data. Acta Botanica Mexicana. 2002, 61: 9-25.Google Scholar
- Hawkes JG: The Potato: Evolution, Biodiversity and Genetic Resources. 1990, Smithsonian Institution Press, Washington, D. CGoogle Scholar
- Spooner DM, Sytsma KJ: Reexamination of the series relationships of Mexican and Central American wild potatoes (Solanum sect. Petota): evidence fromchloroplast DNA restriction site variation. Syst Bot. 1992, 17 (3): 432-448. 10.2307/2419483.View ArticleGoogle Scholar
- Matsubayashi M: Phylogenetic relationships in the potato and its related species. Chromosome Engineering in Plants: Genetics, Breeding, Evolution. Part B. Edited by: Tsuchiya T, Gupta PK. 1991, Elsevier Science, Amsterdam, 93-118. 1Google Scholar
- Bonierbale MW, Plaisted RL, Tanksley SD: RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics. 1988, 120 (4): 1095-1103.PubMedPubMed CentralGoogle Scholar
- Tanksley SD, Ganal MW, Prince JP, Devicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Röder MS, Wing RA, Wu W, Young ND: High-density molecular linkage maps of tomato and potato genomes. Genetics. 1992, 132 (4): 1141-1160.PubMedPubMed CentralGoogle Scholar
- Livingstone KD, Lackney VK, Blauth JR, van Wijk R, Jahn MK: Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics. 1999, 152 (3): 1183-1202.PubMedPubMed CentralGoogle Scholar
- RA P’, Ji Y, Chetelat RT: Comparative linkage map of the Solanum lycopersicoides and S. sitiens genomes and their differentiation from tomato. Genome. 2002, 45 (6): 1003-1012. 10.1139/g02-066.View ArticleGoogle Scholar
- Peters SA, Bargsten JW, Szinay D, van de Belt J, Visser RGF, Bai Y, de Jong H: Structural homology in the Solanaceae: analysis of genomic regions in support of synteny in tomato, potato and pepper. Plant J. 2012, 71 (4): 602-614. 10.1111/j.1365-313X.2012.05012.x.PubMedView ArticleGoogle Scholar
- Sharma SK, Bolser D, de Boer J, Sonderkaer M, Amoroso W, Carboni MF, D’Ambrosio JM, de la Cruz G, Di Genova A, Douches DS, Eguiluz M, Guo X, Guzman F, Hackett CA, Hamilton JP, Li G, Li Y, Lozano R, Maass A, Marshall D, Martinez D, McLean K, Mejía N, Milne L, Munive S, Nagy I, Ponce O, Ramirez M, Simon R, Thomson SJ, et al: Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. G3. 2013, 3 (11): 2031-2047. 10.1534/g3.113.007153.PubMedPubMed CentralView ArticleGoogle Scholar
- Szinay D, Wijnker E, van den Berg R, Visser RGF, de Jong H, Bai Y: Chromosome evolution in Solanum traced by cross-species BAC-FISH. New Phytol. 2013, 195 (3): 688-698. 10.1111/j.1469-8137.2012.04195.x.View ArticleGoogle Scholar
- Iovene M, Wielgus SM, Simon PW, Buell CR, Jiang J: Chromatin structure and physical mapping of chromosome 6 of potato and comparative analyses with tomato. Genetics. 2008, 180 (3): 1307-1317. 10.1534/genetics.108.093179.PubMedPubMed CentralView ArticleGoogle Scholar
- Consortium TG: The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012, 485 (7400): 635-641. 10.1038/nature11119.View ArticleGoogle Scholar
- Bradeen JM, Naess SK, Song J, Haberlach GT, Wielgus SM, Buell CR, Jiang J, Helgeson JP: Concomitant reiterative BAC walking and fine genetic mapping enable physical map development for the broad-spectrum late blight resistance region, RB. Mol Genet Genomic. 2003, 269 (5): 603-611. 10.1007/s00438-003-0865-8.View ArticleGoogle Scholar
- Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A: Diversity Arrays Technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci U S A. 2004, 101 (26): 9915-9920. 10.1073/pnas.0401076101.PubMedPubMed CentralView ArticleGoogle Scholar
- Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C, Aschenbrenner-Kilian M, Evers M, Peng K, Cayla C, Hok P, Uszynski G: Diversity Arrays Technology (DArT) - a generic genome profiling technology on open platforms. Data Production and Analysis in Population Genomics. Edited by: Pompanon F, Bonin A. 2012, Humana Press, New York, 67-91. 10.1007/978-1-61779-870-2_5. Series: Methods in Molecular Biology, vol 888View ArticleGoogle Scholar
- Wittenberg AHJ, van der Lee T, Cayla C, Kilian A, Visser RGF, Schouten HJ: Validation of the high-throughput marker technology DArT using the model plant Arabidopsis thaliana . Mol Genet Genomics. 2005, 274 (1): 30-39. 10.1007/s00438-005-1145-6.PubMedView ArticleGoogle Scholar
- Akbari M, Wenzl P, Caig V, Carling J, Xia L, Yang SY, Uszynski G, Mohler V, Lehmensiek A, Kuchel H, Hayden MJ, Howes N, Sharp P, Vaughan P, Rathmell B, Huttner E, Kilian A: Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet. 2006, 113 (8): 1409-1420. 10.1007/s00122-006-0365-4.PubMedView ArticleGoogle Scholar
- Sliwka J, Jakuczun H, Chmielarz M, Hara-Skrzypiec A, Tomczynska I, Kilian A, Zimnoch-Guzowska E: A resistance gene against potato late blight originating from Solanum X michoacanum maps to potato chromosome VII. Theor Appl Genet. 2012, 124 (2): 397-406. 10.1007/s00122-011-1715-4.PubMedPubMed CentralView ArticleGoogle Scholar
- Sliwka J, Jakuczun H, Chmielarz M, Hara-Skrzypiec A, Tomczynska I, Kilian A, Zimnoch-Guzowska E: Late blight resistance gene from Solanum ruiz-ceballosii is located on potato chromosome X and linked to violet flower colour. BMC Genet. 2012, 13: 11-10.1186/1471-2156-13-11.PubMedPubMed CentralView ArticleGoogle Scholar
- Bradeen JM, Iorizzo M, Mann H, Gao L, D’Agostino N, Chiusano ML, Carputo D: DArT markers for linkage mapping and cross-species comparison of genome structures. Proceedings of the he 2010 ASHS Annual Conference. 2010, Palm desert, CA (USA)Google Scholar
- Traini A, Iorizzo M, Mann H, Bradeen JM, Carputo D, Frusciante L, Chiusano ML: Genome microscale heterogeneity among wild potatoes revealed by Diversity Arrays Technology marker sequences. Int J Genomics 2013, 257218. doi:10.1155/2013/2572218.,Google Scholar
- Consortium PGS: Genome sequence and analysis of the tuber crop potato. Nature. 2011, 475 (7355): 189-195. 10.1038/nature10158. Advance online publicationView ArticleGoogle Scholar
- Ritter E, Gebhardt C, Salamini F: Estimation of recombination frequencies and construction of RFLP linkage maps in plants from cresses between henterozygous parents. Genetics. 1990, 125 (3): 645-654.PubMedPubMed CentralGoogle Scholar
- Mann H, Iorizzzo M, Gao L, D’Agostino N, Carputo D, Chiusano ML, Bradeen JM: Molecular linkage maps: strategies, resources and achievements. Genetic, Genomics and Breeding of Potato. Edited by: Bradeen JM, Kole C. 2011, CRC Press/Science Publishers, Enfield, NH, USA, 68-89. 10.1201/b10881-5. Series: Genetics, Genomics and Breeding of Crop Plants ,View ArticleGoogle Scholar
- Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schachtschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F: RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor Appl Genet. 1991, 83 (1): 49-57. 10.1007/BF00229225.PubMedView ArticleGoogle Scholar
- Marks GE: Cytogenetic studies in tuberous Solanum species: I. Genomic differentiation in the group Demissa. J Genetics. 1955, 53 (2): 262-269. 10.1007/BF02993980.View ArticleGoogle Scholar
- Hawkes JG: Taxonomy, cytology and crossability. Kartoffel (Potato). Edited by: Kappert H, Rudorf W. 1958, Handbuch der Pflanzenzüchtung;, Berlin, 1-43.Google Scholar
- Irikura Y: Cytogenetic studies on the haploid plants of tuber-bearing Solanum species: II. Cytogenetic investigations on haploid plants and interspecific hybrids by utilizing haploidy. 1976, National Agricultural Research Station, Hokkaido, JapanGoogle Scholar
- Ramanna MS, Hermsen JGT: Genome Relationships in tuber-bearing Solanums . The biology and taxonomy of the Solanceae. Edited by: Hawkes JG, Lester RN, Skelding AD. 1979, Academic Press, New York, 647-657.Google Scholar
- Hermsen JGT, Ramanna MS: Barriers to hybridization of Solanum bulbocastanum Dun. and S. verrucosum Schlechtd. and structural hybridity in their F1 plants. Euphytica. 1976, 25 (1): 1-10. 10.1007/BF00041523.View ArticleGoogle Scholar
- Rodriguez F, Spooner DM: Nitrate reductase phylogeny of potato (Solanum sect. Petota) genomes with emphasis on the origins of the polyploid species. Syst Bot. 2009, 34 (1): 207-219. 10.1600/036364409787602195.View ArticleGoogle Scholar
- Spooner DM, Rodriguez F, Polgar Z, Ballard HEJ, Jansky SH: Genomic origins of potato polyploids: GBSSI gene sequencing data. Crop Sci. 2008, 48 (Suppl 1): 27-36.Google Scholar
- Aversano R, Ercolano MR, Frusciante L, Monti L, Bradeen JM, Cristinzio G, Zoina A, Greco N, Vitale S, Carputo D: Resistance traits and AFLP characterization of dipoid primitive tuber-bearing potatoes. Genet Resour Crop Evol. 2007, 54 (8): 1797-1806. 10.1007/s10722-006-9201-6.View ArticleGoogle Scholar
- Rouppe van der Voort JNAM, Janssen GJW, Overmars H, van Zandvoort PM, van Norel A, Scholten OE, Janssen R, Bakker J: Development of a PCR-based selection assay for root-knot nematode resistance (Rmc1) by a comparative analysis of the Solanum bublocastanum and S. tuberosum genome. Euphytica. 1999, 106: 187-195. 10.1023/A:1003587807399.View ArticleGoogle Scholar
- Sanchez MJ, Bradeen JM: Towards efficient isolation of R gene orthologs from multiple genotypes: optimization of Long Range-PCR. Mol Breed. 2006, 17 (2): 137-148. 10.1007/s11032-005-4475-5.View ArticleGoogle Scholar
- Quirin EA, Mann H, Meyer RS, Traini A, Chiusano ML, Litt A, Bradeen JM: Evolutionary meta-analysis of Solanaceous resistance gene and Solanum resistance gene analog sequences and a practical framework for cross-species comparisons. Mol Plant Microb Interact. 2012, 25: 603-612. 10.1094/MPMI-12-11-0318-R.View ArticleGoogle Scholar
- Fulton T, Chunwongse J, Tanksley S: Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Bio Rep. 1995, 13 (3): 207-209. 10.1007/BF02670897.View ArticleGoogle Scholar
- Gremme G, Brendel V, Sparks ME, Kurtz S: Engineering a software tool for gene structure prediction in higher organisms. Inf Softw Technol. 2005, 47 (15): 965-978. 10.1016/j.infsof.2005.09.005.View ArticleGoogle Scholar
- Voorrips RE: MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered. 2002, 93 (1): 77-78. 10.1093/jhered/93.1.77.PubMedView ArticleGoogle Scholar
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