Abstract
Solanum section Petota is taxonomically difficult, partly because of interspecific hybridization at both the diploid and polyploid levels. The taxonomy of cultivated potatoes is particularly controversial. Using DNA sequence data of the waxy gene, we here infer relationships among the four species of cultivated potatoes accepted in the latest taxonomic treatment (S. ajanhuiri, S. curtilobum, S. juzepczukii and S. tuberosum, the latter divided into the Andigenum and Chilotanum Cultivar Groups). The data support prior ideas of hybrid origins of S. ajanhuiri from the S. tuberosum Andigenum Group (2x = S. stenotomum) × S. megistacrolobum; S. juzepczukii from the S. tuberosum Andigenum Group (2x = S. stenotomum) × S. acaule; and S. curtilobum from the S. tuberosum Andigenum Group (4x = S. tuberosum subsp. andigenum) × S. juzepczukii. For the tetraploid cultivar-groups of S. tuberosum, hybrid origins are suggested entirely within much more closely related species, except for two of three examined accessions of the S. tuberosum Chilotanum Group that appear to have hybridized with the wild species S. maglia. Hybrid origins of the crop/weed species S. sucrense are more difficult to support and S. vernei is not supported as a wild species progenitor of the S. tuberosum Andigenum Group.
Similar content being viewed by others
References
Adams KL, Wendel JF (2005) Novel patterns of gene expression in polyploid plants. Trends Genet 21:539–543
Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168:2217–2226
Adiwilaga KD, Brown CR (1991) Use of 2n pollen-producing triploid hybrids to introduce tetraploid Mexican wild species germ plasm to cultivated tetraploid potato gene pool. Theor Appl Genet 81:645–662
Alvarez NMB, Peralta IE, Salas A, Spooner DM (2008) A morphological study of species boundaries of the wild potato Solanum brevicaule complex: replicated field trials in Peru. Plant Syst Evol 274:37–45
Ames M, Spooner DM (2008) DNA from herbarium specimens settles a controversy about origins of the European potato. Am J Bot 95:252–257
Astley D, Hawkes JG (1979) The nature of the Bolivian weed potato species Solanum sucrense Hawkes. Euphytica 28:685–696
Baum DA (2007) Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon 56:417–426
Bradshaw J, Bryan G, Ramsay G (2006) Genetic resources (including wild and cultivated Solanum species) and progress in their utilisation in potato breeding. Potato Res 49:49–65
Brickell CD, Alexander C, David JC, Hetterscheid WLA, Leslie AC, Malecot V, Jin X (2009) International Code of Nomenclature for Cultivated Plants, 8th edn. Scripta Hort 10:1–204
Brücher H (1964) El origen de la papa (Solanum tuberosum): nuevas consideraciones sobre un antiguo problema. Physis 68:439–452
Bukasov SM (1971) Cultivated potato species. In: Bukasov SM (ed) Flora of cultivated plants, vol IX. Kolos, Leningrad, Russia, pp 5–40
Camadro EL, Espinillo JC (1990) Germplasm transfer from the wild tetraploid species Solanum acaule Bitt. to the cultivated potato S. tuberosum L. using 2n eggs. Am Potato J 67:737–749
Carputo D, Barone A (2005) Ploidy manipulations in potato through sexual hybridization. Ann Appl Biol 146:71–79
Carputo D, Barone A, Frusciante L (2000) 2n gametes in the potato: essential ingredients for breeding and germplasm transfer. Theor Appl Genet 101:805–813
Carputo D, Frusciante L, Peloquin SJ (2003a) The role of 2n gametes and endosperm balance number in the origin and evolution of polyploids in the tuber-bearing Solanums. Genetics 163:287–294
Carputo D, Parisi M, Consiglio F, Iovene M, Caruso G, Monti L, Frusciante L (2003b) Aneuploid hybrids from 5x–4x crosses in potato: chromosome number, fertility, morphology and yield. Am J Potato Res 80:93–101
Darmo E, Peloquin SJ (1990) Performance and stability of nine tetraploid clones from tetraploid-diploid crosses and four commercial cultivars. Potato Res 33:357–364
De Maine M, Carroll CP, Torrance CJW (1993) Culinary quality of tubers derived from Solanum phureja and S. tuberosum × S. phureja hybrids. J Agric Sci 120:213–217
Dodds KS (1962) Classification of cultivated potatoes. In: Correll (ed) The potato and its wild relatives. Vol 4. Contributions from the Texas Research Foundation, Botanical Studies, Texas, pp 517–539
Ducreux LJM, Morris WL, Prosser IM, Morris JA, Beale MH, Wright F, Shepherd T, Bryan GJ, Hedley PE, Taylor MA (2008) Expression profiling of potato germplasm differentiated in quality traits leads to the identification of candidate flavour and texture genes. J Exp Bot 59:4219–4231
Farris JS (1970) Methods for computing Wagner trees. Syst Zool 19:83–92
Felsenstein J (1973) Maximum likelihood and minimum-steps methods for estimating evolutionary trees from data on discrete characters. Syst Zool 22:240–249
Flagel L, Udall J, Nettleton D, Wendell J (2008) Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6:16
Grun P (1990) The evolution of the cultivated potatoes. Econ Bot 44(Suppl 3):39–55
Hanneman RE Jr (1994) Assignment of endosperm balance numbers to the tuber-bearing Solanums and their close non-tuber-bearing relatives. Euphytica 74:19–25
Hawkes JG (1990) The potato: evolution, biodiversity and genetic resources. Belhaven Press, Oxford, UK
Hijmans RJ, Jacobs M, Bamberg JB, Spooner DM (2003) Frost tolerance in wild potato species: assessing the predictivity of taxonomic, geographic, and ecological factors. Euphytica 130:47–59
Hosaka K (2002) Distribution of the 241 bp deletion of chloroplast DNA in wild potato species. Am J Potato Res 79:119–123
Hosaka K (2003) T-type chloroplast DNA in Solanum tuberosum L. ssp. tuberosum was conferred from some populations of S. tarijense Hawkes. Am J Potato Res 80:21–32
Hovav R, Chaudhary B, Udall JA, Flagel L, Wendel JF (2008a) Parallel domestication, convergent evolution and duplicated gene recruitment in allopolyploid cotton. Genetics 179:1725–1733
Hovav R, Udall JA, Chaudhary B, Rapp R, Flagel L, Wendel JF (2008b) Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant. Proc Natl Acad Sci USA 105:6191–6195
Huamán Z, Spooner DM (2002) Reclassification of landrace populations of cultivated potatoes (Solanum sect. Petota). Am J Bot 89:947–965
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Johns T, Alonso JG (1990) Glycoalkaloid change during the domestication of the potato, Solanum section Petota. Euphytica 50:203–210
Johnston SA, Hanneman RE Jr (1982) Manipulations of endosperm balance number overcome crossing barriers between diploid Solanum species. Science 217:446–448
Lechnovich VS (1971) Cultivated potato species. In: Bukasov SM (ed) Flora of cultivated plants, Chap 2, vol IX. Kolos, Leningrad, pp 41–304
Maddison DR, Maddison WP (2001) MacClade 4.03: Analysis of phylogeny and character evolution, v. 4.08. Sinauer Associates, Sunderland
Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230
McNeill J, Barrie FR, Burdet HM, Demoulin V, Hawksworth DL, Marhold K, Nicolson DH, Prado J, Silva PC, Skog JE, Wiersema JH, Turland NJ (2006) International Code of Botanical Nomenclature (Vienna Code). Regnum Veg 146:1–568
Mendiburu AO, Peloquin SJ (1977) Bilateral sexual polyploidization in potatoes. Euphytica 26:573–583
Miller JT, Spooner DM (1999) Collapse of species boundaries in the Solanum brevicaule complex (Solanaceae: S. sect. Petota): molecular data. Plant Syst Evol 214:103–130
Morris WL, Ross HA, Ducreux JM, Bradshaw J, Bryan GJ, Taylor MA (2007) Umami compounds are a determinant of the flavor of potato (Solanum tuberosum L.). J Agric Food Chem 55:9627–9633
Morris WL, Ducreux LJM, Bryan GJ, Taylor MA (2008) Molecular dissection of sensory traits in the potato tuber. Am J Potato Res 85:286–297
Müller KF (2005) SeqState-primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinform 4:65–69
Ochoa CM (1990) The potatoes of South America: Bolivia. Cambridge University Press, Cambridge
Ochoa CM (1999) Las papas de Sudamerica: Perú. Centro International de La Papa (CIP), Lima, Perú
Olmstead RG, Palmer JD (1994) Chloroplast DNA and systematics: a review of methods and data analysis. Am J Bot 81:1205–1224
Ortiz R (1998) Potato breeding via ploidy manipulations. Plant Breed Rev 16:15–86
Ortiz R, Freyre R, Peloquin SJ, Iwanaga M (1991) Adaptation to day length and yield stability of families from tetraploid × diploid crosses in potato. Euphytica 56:187–195
Peloquin SJ, Boiteux LS, Carputo D (1999) Meiotic mutants in potato: valuable variants. Genetics 153:1493–1499
Pendinen G, Gavrilenko T, Jiang J, Spooner DM (2008) Allopolyploid speciation of the tetraploid Mexican potato species S. stoloniferum and S. hjertingii revealed by genomic in situ hybridization. Genome 51:714–772
Peralta IE, Spooner DM (2001) GBSSI gene phylogeny of wild tomatoes (Solanum L. section Lycopersicon [Mill.] Wettst. subsection Lycopersicon). Am J Bot 88:1888–1902
Plaisted RL, Hoopes RW (1989) The past record and future prospects for the use of exotic potato germplasm. Am Potato J 66:603–627
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Raker C, Spooner DM (2002) The Chilean tetraploid cultivated potato, Solanum tuberosum, is distinct from the Andean populations; microsatellite data. Crop Sci 42:1451–1458
Rios D, Ghislain M, Rodríguez F, Spooner DM (2007) What is the origin of the European potato? Evidence from Canary Island landraces. Crop Sci 47:1271–1280
Rodríguez F, Spooner DM (2009) Nitrate reductase phylogeny of potato (Solanum sect. Petota) genomes with emphasis on the origins of the polyploid species. Syst Bot 34:207–219
Rodríguez F, Wu F, Ané C, Tanksley S, Spooner DM (2009) Do potatoes and tomatoes have a single evolutionary history, and what proportion of the genome supports this history? BMC Evol Biol 9:191
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381
Spooner DM (2009) DNA barcoding will frequently fail in complicated groups: an example in wild potatoes. Am J Bot 96:1177–1189
Spooner DM, Castillo R (1997) Reexamination of series relationships of South American wild potatoes (Solanaceae: Solanum sect. Petota): evidence from chloroplast DNA restriction site variation. Am J Bot 84:671–685
Spooner DM, van den Berg RG (1992) An analysis of recent taxonomic concepts in wild potatoes (Solanum sect. Petota). Gen Res Crop Evol 39:23–37
Spooner DM, Anderson GJ, Jansen RK (1993) Chloroplast DNA evidence for the interrelationships of tomatoes, potatoes, and pepinos (Solanaceae). Am J Bot 80:676–688
Spooner DM, McLean K, Ramsay G, Waugh R, Bryan GJ (2005) A single domestication for potato based on multilocus AFLP genotyping. Proc Natl Acad Sci USA 102:14694–14699
Spooner DM, Fajardo D, Bryan GJ (2007a) Species limits of Solanum berthaultii Hawkes and S. tarijense Hawkes and the implications for species boundaries in Solanum sect. Petota. Taxon 56:987–999
Spooner DM, Núñez J, Trujillo G, del Rosario Herrera M, Guzmán F, Ghislain M (2007b) Extensive simple sequence repeat genotyping of potato landraces supports a major reevaluation of their gene pool structure and classification. Proc Natl Acad Sci USA 104:19398–19403
Spooner DM, Rodríguez F, Polgár Z, Ballard Jr HE, Jansky SH (2008) Genomic origins of potato polyploids: waxy gene sequencing data. Plant Genome Suppl Crop Sci 48(S1):S27–S36
Spooner DM, Ames M, Fajardo D, Rodríguez F (2009) Species boundaries and interrelationships of Solanum sect. Petota (wild and cultivated potatoes) are drastically altered as a result of PBI-funded research. Botany and Mycology 2009 Meeting Abstracts. http://2009.botanyconference.org/engine/search/index.php?func=detail&aid=24
Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241
Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4.0b3a PPC. Sinauer Associates, Sunderland
Tai GCC (1976) Estimation of general and specific combining abilities in potato. Can J Genet Cytol 18:463–470
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Ugent D (1970) The potato. Science 179:1161–1166
Van den Berg RG, Miller JT, Ugarte ML, Kardolus JP, Villand J, Nienhuis J, Spooner DM (1998) Collapse of morphological species in the wild potato Solanum brevicaule complex (Solanaceae: sect. Petota). Am J Bot 85:92–109
Wang J, Tian L, Madlung A, Lee H-S, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:1961–1973
Watanabe K, Peloquin SJ, Endo M (1991) Genetic significance of mode of polyploidization: somatic doubling or 2n gametes? Genome 34:28–34
Werner JE, Peloquin SJ (1991) Significance of allelic diversity and 2n gametes for approaching maximum heterozygosity in 4x potatoes. Euphytica 58:21–29
Winfield M, Lloyd D, Griffiths W, Bradshaw J, Muir D, Nevison I, Bryan G (2005) Assessing organoleptic attributes of Solanum tuberosum and S. phureja potatoes. Aspects Appl Biol 76:127–135
Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724
Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. thesis. The University of Texas, Austin
Acknowledgments
This study was supported by NSF DEB 0316614 entitled PBI Solanum: a worldwide treatment (http://www.nhm.ac.uk/researchcuration/projects/solanaceaesource//) to DS and by the USDA National Research Initiative Grant 2008-35300-18669 to DS.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Bryan.
Rights and permissions
About this article
Cite this article
Rodríguez, F., Ghislain, M., Clausen, A.M. et al. Hybrid origins of cultivated potatoes. Theor Appl Genet 121, 1187–1198 (2010). https://doi.org/10.1007/s00122-010-1422-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-010-1422-6