• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Oct 11, 2005; 102(41): 14694–14699.
Published online Oct 3, 2005. doi:  10.1073/pnas.0507400102
PMCID: PMC1253605
Evolution

A single domestication for potato based on multilocus amplified fragment length polymorphism genotyping

Abstract

The cultivated potato, Solanum tuberosum, ultimately traces its origin to Andean and Chilean landraces developed by pre-Colombian cultivators. These Andean landraces exhibit tremendous morphological and genetic diversity, and are distributed throughout the Andes, from western Venezuela to northern Argentina, and in southern Chile. The wild species progenitors of these landraces have long been in dispute, but all hypotheses center on a group of ≈20 morphologically very similar tuber-bearing (Solanum section Petota) wild taxa referred to as the S. brevicaule complex, distributed from central Peru to northern Argentina. We present phylogenetic analyses based on the representative cladistic diversity of 362 individual wild (261) and landrace (98) members of potato (all tuber-bearing) and three outgroup non-tuber-bearing members of Solanum section Etuberosum, genotyped with 438 robust amplified fragment length polymorphisms. Our analyses are consistent with a hypothesis of a “northern” (Peru) and “southern” (Bolivia and Argentina) cladistic split for members of the S. brevicaule complex, and with the need for considerable reduction of species in the complex. In contrast to all prior hypotheses, our data support a monophyletic origin of the landrace cultivars from the northern component of this complex in Peru, rather than from multiple independent origins from various northern and southern members.

Keywords: evolution, sect. Petota, Solanum

The origin of crop plants has long fascinated botanists, archaeologists, and sociologists with the following fundamental questions: When, where, how, why, and how many times did crop domestication occur? What are the wild progenitors of these crops? How do crops differ from their progenitors, what selective processes, and how many genetic changes produce these changes? Did crops have single or multiple and separate origins (1-5)? Single (diffusionist) vs. multiple origin (in situ) hypotheses of crop origins has long been the subject of debate (6-8). We have used multilocus molecular data from amplified fragment length polymorphisms (AFLPs) to reassess a single vs. multiple origin of landrace cultivars of cultivated potato.

Primitive indigenous cultivated (landrace) potatoes are widely distributed in the Andes from western Venezuela south to northern Argentina, and in Chiloé Island and the adjacent Chonos Archipelago of south-central Chile. The Chilean landraces are secondarily derived from the Andean ones (9), likely after hybridization with the Bolivian and Argentinean species Solanum tarijense (10). Potato landraces have been classified into 21 species (11, 12), 7 species (9), 9 species (13, 14), or as a single species, S. tuberosum, with eight cultivar groups (15). The landraces are very diverse, with hundreds of clones differing in tuber colors and shapes, and leaf, floral, and growth habit variations. Ploidy levels in cultivated potato range from diploid (2n = 2x = 24), to triploid (2n = 3x = 36), to tetraploid (2n = 4x = 48), to pentaploid (2n = 5x = 60). The wild relatives of these landraces (Solanum section Petota) are all tuber-bearing and include ≈190 wild species that are widely distributed in the Americas from the southwestern United States to southern Chile (16, 17); they possess all ploidy levels of the cultivars, as well as hexaploids (2n = 6x = 72).

The wild species progenitors of these Andean landraces have long been in dispute, but all hypotheses center on a group of ≈20 morphologically similar wild species referred to as the S. brevicaule complex, distributed from central Peru to northern Argentina (18-22). Members of the complex are morphologically similar to the landraces. Potato domestication from these wild species involved selection for underground characters of shorter stolons, larger tubers, (often) colored and variously shaped tubers, and the reduction of bitter tuber glycoalkaloids; above-ground characters of wild and cultivated species are similar but with cultivated types exhibit high vigor and extensive segregation for flower and foliage traits. The S. brevicaule complex includes diploids, tetraploids, and hexaploids. Many members grow as weeds in or adjacent to cultivated potato fields and form crop-weed complexes (19). Morphological data (21) and single- to low-copy nuclear restriction fragment length polymorphism data (22) failed to clearly differentiate wild species in the S. brevicaule complex from each other or from most landraces (although the landraces often are taller and more vigorous as a group than the wild species), and the most liberal taxonomic interpretation from these studies was to recognize only three wild taxa: (i) the Peruvian populations of the S. brevicaule complex, (ii) the Bolivian and Argentinean populations of the S. brevicaule complex, and (iii) S. oplocense (Bolivia and Argentina).

Literally all hypotheses have suggested complex hybrid or multiple origins of the cultivars from both northern and southern members of the S. brevicaule complex (9, 13-15, 19-21, 23-25). This study investigates these hypotheses through phylogenetic analyses that incorporate the first comprehensive sampling of landraces, the putative progenitors, and outgroups.

Materials and Methods

Plant Materials. We sampled 362 individual wild (261) and landrace (98) members of tuber-bearing relatives of potato (Solanum section Petota) and three sister group representatives in Solanum section Etuberosum (S. etuberosum and S. palustre). These accessions came from the United States Potato Genebank (www.ars-grin.gov/nr6) and the Commonwealth Potato Collection of the Scottish Crop Research Institute (www.scri.ac.uk/cpc). They were identified mostly from living accessions planted at the genebank by visiting potato taxonomists (mainly Jack Hawkes and Carlos Ochoa) over 30 years. The 264 wild species accessions are mostly members of the S. brevicaule complex and are largely the same ones used in prior morphological (21) and molecular (22) studies of the complex, and are labeled as those species. We included tetraploid S. stoloniferum to have a data set comparable to the prior morphological and molecular studies. The members of the S. brevicaule complex are so similar that their identities have frequently changed, and we mostly use the identities from these prior studies for consistency. We add additional cultivated accessions and wild species to represent the entire four-clade diversity of section Petota from Spooner and Castillo (26), and they included members of the Phureja Group (diploid, Andean), Stenotomum Group (diploid, Andean), Andigenum Group (tetraploid, Andean), and Chilotanum group (tetraploid, lowland Chile). Our study included 230 diploids (2n = 2x = 24), 120 tetraploids (2n = 4x = 48), and 12 hexaploids (2n = 6x = 72). S. gourlayi included its diploid and tetraploid cytotypes, and S. oplocense included its tetraploid and hexaploid cytotypes. Designations of ploidy and classes of species (cultivated, S. brevicaule group north, S. brevicaule south, outgroups, and ploidy) are presented in Fig. 1.

Fig. 1.Fig. 1.
Strict consensus parsimony cladogram of 10,000 equally parsimonious 13,176-step Wagner trees based on the entire AFLP data set of 362 accessions, with six AFLP primer combinations producing 438 characters. Outgroups consist of three accessions in Solanum ...

AFLP Genotyping. Plants were grown in the glasshouse, and DNA was extracted from frozen plant leaf tissue taken from single plants by using the DNeasy Plant DNA Extraction kit (Qiagen, cat. no. 69181). AFLP assays were performed by using a modification of the protocol of Vos et al. (27), using the 6-bp cutting enzymes PstI and EcoRI and the 4-bp cutting enzyme MseI. The six AFLP primer combinations used were EAAC + MCCA, EACA + MCAC, PAC + MACT, PAG + MACC, PAT + MAAC, and PCA + MAGG. PCR reactions were set up on 384-well plates by using a Beckman Biomek 2000 liquid handling device. Electrophoresis was carried out on the Bio-Rad Sequi-Gen GT system on 5% acrylamide and 7 M urea in 1× TBE buffer (100 mM Tris/100 mM boric acid/2 mM EDTA). A dual buffer system of 1× TBE and 1× TBE supplemented with 0.5 M NaOAc was used to create an ionic gradient, which resulted in better separation of the larger fragments. A Promega fmol DNA Cycle Sequencing system (Promega Q4100) marker (prepared according to the protocol but using only d/ddT Nucleotide Mix) was run to estimate fragment sizes. Gels were dried onto paper and visualized by exposure to x-ray film (Kodak BIOMAX MR). Gels were scanned by using a standard flat-bed scanner at 300 dpi and 8-bit grayscale format. The TIFF images were then imported into aflp-quantar software supplied by Keygene (Wageningen, The Netherlands). To enable automatic positioning of marker bands, a standard genotype was run on each gel. The AFLP data matrices are published as supporting information on the PNAS web site.

Phylogenetic Analysis. Phylogenetic reconstructions were performed by using paup* 4.0b8 (28), using Wagner parsimony (29). The non-tuber-bearing species S. etuberosum and S. palustre (section Etuberosum) were designated as the outgroup, but members of these species, and clades 1, 2, and 3 of Spooner and Castillo (26), fall at the base of the tree and are listed as outgroups in Fig. 1; all remaining wild and cultivated species are members of clade 4. To find multiple tree islands, we used a four-step search strategy, modified from Olmstead and Palmer (30). (i) One million replicates initially were run by using random order entry starting trees with nearest-neighbor interchange. (ii) The shortest trees from this analysis were used individually as starting trees with the tree-bisection-reconnection (TBR) method. (iii) The resulting trees were searched with nearest-neighbor interchange, retaining all most parsimonious trees (MULPARS). (iv) The resulting trees were searched with TBR and MULPARS. The last two analyses were terminated at 10,000 trees. The resulting trees were used to compute a strict consensus tree. A bootstrap analysis was conducted on 500 replicates with TBR and MULPARS. The above analyses were done twice, once with the entire data set and again only with the diploids.

AFLP data were also analyzed by neighbor-joining using ntsys-pcR 2.02k (31). The program simqual was used to compute similarity matrices using the “Jaccard” option, which ignores shared absent bands, and which is an appropriate algorithm for AFLPs scored as dominant markers.

Concordance Tests Among the Present AFLP Data to the Prior Restriction Fragment Length Polymorphism (RFLP), Randomly Amplified Polymorphic DNA (RAPD), and Morphological Studies. We tested concordance among our new AFLP results to the morphological (21) and single- to low-copy RFLP and RAPD data (22) of the S. brevicaule complex. For each data set, we constructed parallel matrices containing accessions in common between studies. We then made pairwise distance matrices for all four data sets. For the AFLP and RAPD data, we used the Jaccard matrix, for the RFLP data we used a simple-matching coefficient, and for the morphological data we used the distance algorithm, all present in ntsys-pcR 2.02k (31). We then performed pairwise comparisons of these matrices with the Mantel test (32) as performed in ntsys-pcR. This statistic varies from 0 (no correspondence of matrices) to 1 (perfect correspondence).

Results and Discussion

Cladistic Results. The six AFLP primer combinations produced 438 characters of which 3.6% of the data matrix had missing values, caused by occasional failed reactions or faint bands. Wagner parsimony analysis of all 362 accessions (Fig. 1) produced 10,000 (our designated upper tree limit) most parsimonious 13,672-step trees with a consistency index of 0.033 and a retention index of 0.571, and a rescaled consistency index of 0.019. The topology of the entire data set is very similar to the four clade cladistic structure of Spooner and Castillo (26). S. etuberosum and S. palustre form a monophyletic basal outgroup, sister to S. bulbocastanum, S. polyadenium, S. stenophyllidium, and S. tarnii (clades 1 and 2), sister to S. acroscopicum, S. andreanum, S. chilliasense, S. pascoense, and S. paucissectum (clade 3); this clade also includes two accessions of S. acroscopicum and two accessions of S. multidissectum, members of the S. brevicaule group. The bootstrap analysis (Fig. 1) showed >50% support for the basal clades of sect. Etuberosum and clades 1-3, and in some internal branches of clade 4, but poor support (<50%) in the external branches of clade 4. Wagner parsimony analysis of the 230 diploid accessions (data not shown) produced 177 most parsimonious 8,393-step trees with a consistency index of 0.0534, and a retention index of 0.5617 and a rescaled consistency index of 0.0300; bootstrap support was similar to the total taxon tree. The topology of the entire data set and the reduced data set of the diploids differs very little.

The topology of the entire data set is in concordance with the morphological (21), RAPD, and RFLP results (22) in defining a northern (species from Peru, together with S. achacachense from northern Bolivia) and southern (species from Bolivia and northern Argentina) clade of the S. brevicaule complex. This geographic split does not exactly follow country borders, but very closely so. For example, the northern clade contains S. achacachense PI 558032 from the department of La Paz, Bolivia bordering Peru, and the southern clade contains S. leptophyes PI 458378 from the department of Puno bordering Bolivia.

Also in concordance with prior results, the AFLP data fail to resolve many species in the complex. Species that fail to form clades in the northern S. brevicaule group are S. abancayense, S. bukasovii, S. canasense, S. leptophyes, S. marinasense, S. multidissectum, and S. multiinterruptum, whereas S. candolleanum and S. pampasense form clades. Species that fail to form clades in the southern complex are S. ambosinum, S. brevicaule, S. canasense, S. leptophyes, S. oplocense, S. sparsipilum, and S. sucrense, whereas S. avilesii, S. hoopesii, S. incamayoense, S. spegazzinii, S. ugentii, S. vernei, and S. vidaurrei [diploid] (to the exclusion of one accession of S. gourlayi [tetraploid]) form clades.

The AFLP data support a monophyletic origin of all of the cultivars. S. bukasovii 568954 and S. acroscopicum 230495, however, fall within the cultivated clade. Accession 230495 was labeled in the genebank as S. acroscopicum (a diploid species), but chromosome counts show it to be tetraploid and likely to be a misidentified cultivated species. S. bukasovii 568954 could be a progenitor or an unrecognized cultivated diploid species.

Hosaka (10) showed that S. tarijense was a likely maternal contributor in the origin of landraces of the Chilotanum group, because they share a 241-bp chloroplast deletion. Our examination of three accessions of S. tarijense, and the related species S. arnesii, S. berthaultii, and S. chacoense, show them to form a clade, separate from the cultivars.

Phenetic Results. Because AFLPs are dominant and anonymous marker data, a case has been made that they should be analyzed with phenetic methods (33). The neighbor-joining tree (data not shown) outlines nearly the same set of species groups including the northern and southern S. brevicaule groups, places the cultivated species as a single group, and places the outgroup distant to the tuber-bearing species. A phenogram could represent the phylogeny when similarities are mainly due to shared derived characteristics (34). In our case, conclusions are the same with cladistic or neighbor-joining procedures, and controversies of proper methods to use are therefore moot.

Concordance of the Present AFLP Data to Prior Morphological and Molecular Data in the S. brevicaule Complex. The Mantel tests showed high correlations (r) of the present AFLP results to the prior RAPD and single- to low-copy nuclear RFLP results of the S. brevicaule complex (22) (r = 0.740-0.845) (Table 1) and much lower correlations to the morphological data (r = 0.204). Despite much lower correspondence of AFLP, RFLP, and RAPD results to the morphological results (Table 1), the morphological data still showed a north-south partitioning by a canonical variates analysis (21).

Table 1.
Pairwise comparisons of the present AFLP results to the morphological results (21) and RAPD and single- to low-copy nuclear RFLP results (22) using the same accessions, as performed with the Mantel test (32)

The utility of AFLPs to examine relationships of closely related species has been documented elsewhere. For example, Powell et al. (35) showed AFLPs and nuclear RFLPs to be significantly correlated in diversity studies of cultivated soybean (Glycine max [L.] Merrill) and its progenitor species G. soja Hort.; Milbourne et al. (36) showed good correlations between AFLPs and RAPDs in S. tuberosum; and Russell et al. (37) showed good correlations of AFLPs and nuclear RFLPs in Hordeum. Such correlations, and the concordance of AFLP to nuclear RFLP, RAPD, and morphological results reported here, support the utility of AFLPs for examining relationships of S. tuberosum and the S. brevicaule complex.

Single Domestication for Potato. All cladistic and phenetic analyses, of both the diploids and tetraploids, show all landrace populations to form a monophyletic clade, derived from the northern members of the S. brevicaule complex. These S. brevicaule northern group member “species” are poorly defined, and ongoing studies may reduce them to a single species, with the earliest valid name of the group being S. bukasovii. The conclusions of a single origin of cultivated potato from the northern species of the S. brevicaule group differs from all conventional domestication hypotheses (9, 13, 15, 19-21, 23-25) in two fundamental respects: (i) a single origin is here supported, rather than a series of multiple independent origins; and (ii) the origin is confined to the northern component of the S. brevicaule complex, rather than to other southern complex species that are commonly mentioned as progenitors, such as S. sparsipilum or S. vernei (e.g., refs. 9 and 23). A “single” origin is here supported to mean an origin from a single species, or its progenitor (S. bukasovii), in the broad area of southern Peru. Because landrace potatoes are currently spread throughout the Andes and Chile, they clearly were diffused from Peru both north and south, assuming present-day distributions of the original cultivars.

The single origin of potato parallels results suggesting single origins of other crops including barley (38), cassava (39), maize (40), einkorn wheat (41), and emmer wheat (42). This differs from multiple origins of common beans (43), cotton (44), millet (45), rice (46), and squash (47). Allaby and Brown (48) criticize the use of “anonymous” marker data of any type (including AFLPs) to infer single crop origins. Results of computer simulations have led these authors to postulate that monophyletic origins can be erroneously inferred when using dominant marker data analyzed by neighbor-joining methods. They assume that pairs of markers, on average, are unlinked and simulate different scenarios for cereal crops. Authors of some of the original studies have replied, suggesting that the “intrinsic quality” of their data outweighs any doubts through use of simulated data (49). It is clear that further, more sophisticated simulations are required, using information on known marker linkage relationships. Moreover, Allaby and Brown (48) do not comment on the applicability of their studies to predominantly outbreeding, clonally propagated crops, such as potato.

Diamond (50) discusses single vs. multiple crop origins in a geographic perspective. He suggests that crops that spread east and west (as einkorn wheat and emmer wheat in the Fertile Crescent), rather than north and south (as squash and cotton in the Americas), have a competitive advantage in rapid diffusion because they take less time to adapt to new habitats. He further contends that such rapid diffusion preempts adoption of competing crops and favors single crop origins, in contrast to multiple origins of crops spread north and south. His paper was written when maize (51, 52) and potato (present results) were thought to have multiple origins. The widespread north and south diffusion of maize and potatoes, and their monophyletic origin, prompts a reconsideration of his geographic interpretation of single and multiple origins.

Reconsideration of the Taxonomy of the S. brevicaule Complex. The data strongly suggest that (i) considerable reduction of species is needed in the S. brevicaule complex and (ii) the complex is polyphyletic. AFLP data suggest that some of the species in the complex, however (mentioned above), may be valid. AFLP data also suggest, as do the RAPD and nuclear RFLP data, that some accessions of S. multiinterruptum are part of the distinctive clade 3 (series Piurana) (22). Taxonomic changes in species circumscriptions are underway as part of a broader-scale taxonomic revision of the entire genus Solanum (53). Poor support for the traditionally circumscribed S. brevicaule complex species suggests that designations of species-specific progenitors of the landrace cultivars with this outdated taxonomy (9, 25) are futile. Rather, our results suggest that the Andean landrace cultivars arose from the northern component of the S. brevicaule complex. S. bukasovii is the earliest taxonomic name possessing priority as this progenitor.

Supplementary Material

Supporting Data Matrices:

Acknowledgments

We thank the U.S. Department of Agriculture Foreign Agricultural Service and the Scottish Executive Environment and Rural Affairs Department for financial support.

Notes

Abbreviations: AFLP, amplified fragment length polymorphism; RAPD, randomly amplified polymorphic DNA; RFLP, restriction fragment length polymorphism.

References

1. de Candolle, A. (1959) Origin of Crop Plants (reprint of 1886 version) (Hafner Publishing Company, New York).
2. Sauer, C. O. (1969) Agricultural Origins and Dispersals (MIT Press, Cambridge, MA).
3. Hawkes, J. G. (1983) The Diversity of Crop Plants (Harvard Univ. Press, Cambridge, MA).
4. Harlan, J. R. (1992) Crops and Man (ASA/CSSA/SSA, Madison, WI), 2nd Ed.
5. Zohary, D. & Hopf, M. (2000) Domestication of Plants in the Old World (Oxford Univ. Press, Oxford), 3rd Ed.
6. Riley, T. J., Edging, R. & Rossen, J. (1990) Curr. Anthropol. 31, 525-541.
7. Blumer, M. A. (1992) Econ. Bot. 46, 98-111.
8. Zohary, D. (1999) Genet. Resources Crop Evol. 46, 133-142.
9. Hawkes, J. G. (1990) The Potato: Evolution, Biodiversity, and Genetic Resources (Belhaven Press, London).
10. Hosaka, K. (2003) Am. J. Potato Res. 80, 21-32.
11. Bukasov, S. M. (1971) in Flora of Cultivated Plants, ed. Bukasov, S. M. (Kolos, Leningrad, Russia), Vol. 9, pp. 5-40.
12. Lechnovich, V. S. (1971) in Flora of Cultivated Plants, ed. Bukasov, S. M. (Kolos, Leningrad, Russia), Vol. 9, pp. 41-302.
13. Ochoa, C. M. (1990) The Potatoes of South America: Bolivia (Cambridge Univ. Press, Cambridge, U.K.).
14. Ochoa, C. M. (1999) Las Papas de Sudamérica: Perú (International Potato Center, Lima, Peru), Part 1.
15. Huamán, Z. & Spooner, D. M. (2002) Am. J. Bot. 89, 947-965. [PubMed]
16. Spooner, D. M. & Hijmans, R. J. (2001) Am. J. Potato Res. 78, 237-268.
17. Spooner, D. M., van den Berg, R. G., Rodríguez, A., Bamberg, J., Hijmans, R. J. & Lara-Cabrera, S. I. (2004) Syst. Bot. Monogr. 68, 1-209 and nine plates.
18. Correll, D. S. (1962) Contr. Texas Res. Found. Bot. Stud. 4, 1-606.
19. Ugent, D. (1970) Science 170, 1161-1166. [PubMed]
20. Grun, P. (1990) Econ. Bot. 44, Suppl. 3, 39-55.
21. Van den Berg, R. G., Miller, J. T., Ugarte, M. L., Kardolus, J. P., Nienhuis, J. & Spooner, D. M. (1998) Am. J. Bot. 85, 92-109. [PubMed]
22. Miller, J. T. & Spooner, D. M. (1999) Plant Syst. Evol. 214, 103-130.
23. Brücher, H. (1964) Physis (Florence) 24, 439-452.
24. Bukasov, S. M. in Systematics, Breeding, and Seed Production of Potatoes, trans. Dhote, A. K. (1978), ed. Kothetar, V. S. (Amerind, New Dehli), pp. 1-42.
25. Hosaka, K. (1995) Theor. Appl. Genet. 90, 356-363. [PubMed]
26. Spooner, D. M. & Castillo, R. (1997) Am. J. Bot. 84, 671-685. [PubMed]
27. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. & Zabeau, M. (1995) Nucleic Acids Res. 23, 4407-4414. [PMC free article] [PubMed]
28. Swofford, D. L. (2001) paup*: Phylogenetic Analysis Using Parsimony (* and Other Methods) (Sinauer, Sunderland, MA), Version 4.0b8.
29. Farris, J. S. (1970) Syst. Zool. 19, 83-92.
30. Olmstead, R. G. & Palmer, J. D. (1994) Am. J. Bot. 81, 1205-1224.
31. Rohlf, F. J. (1997) ntsys-pc: Numerical Taxonomy and Multivariate Analysis System (Exeter Software, Setauket, NY), Version 2.0.
32. Mantel, N. A. (1967) Cancer Res. 27, 209-220. [PubMed]
33. Koopman, W. J. M., Zevenbergen, M. J. & van den Berg, R. G. (2001) Am. J. Bot. 88, 1881-1887. [PubMed]
34. Futuyma, D. J. (1998) Evolutionary Biology (Sinauer, Sunderland, MA), 3rd Ed.
35. Powell, W., Morgante, M., Andre, C., Hanafey, M., Vogel, J., Tingey, S. & Rafalsky, A. (1996) Mol. Breed. 2, 225-238.
36. Milbourne, D., Meyer, R., Bradshaw, J. E., Baird, E., Bonar, N., Provan, J., Powell, W. & Waugh, R. (1997) Mol. Breed. 3, 127-136.
37. Russell, J. R., Fuller, J. D., Macaulay, M., Hatz, B. G., Jahoor, A., Powell, W. & Waugh, R. (1997) Theor. Appl. Genet. 95, 714-722.
38. Badr, A., Müller, K., Schäfer-Pregl, R., El Rabey, H., Effgen, S., Ibrahim, H. H., Pozzi, C., Rohde, W. & Salamini, F. (2000) Mol. Biol. Evol. 17, 499-510. [PubMed]
39. Olsen, K. M. & Schall, B. A. (2001) Am. J. Bot. 88, 131-142. [PubMed]
40. Matsuoka, Y., Vigouroux, Y., Goodman, M. M., Sanchez-G., J., Buckler, E. & Doebley, J. (2002) Proc. Natl. Acad. Sci. USA 99, 6080-6084. [PMC free article] [PubMed]
41. Heun, M., Schäfer-Pregl, R., Klawan, D., Castagna, R., Accerbi, M., Borghi, B. & Salamini, F. (1997) Science 278, 1312-1314.
42. Özkan, K., Brandolini, A., Schäfer-Pregl, R. & Salamini, F. (2002) Mol. Biol. Evol. 19, 1797-1801. [PubMed]
43. Sonnate, G., Stockton, T., Nodari, R. O., Becerra Velásquez, V. L. & Gepts, P. (1994) Theor. Appl. Genet. 89, 629-635. [PubMed]
44. Wendel, J. F. (1995) in Evolution of Crop Plants, eds. Smart, J. & Simmonds, N. W. (Longman, Essex, U.K.), pp. 358-366.
45. Yabuno, T. (1962) Cytologia 27, 296-305.
46. Second, G. (1982) Jpn. J. Genet. 57, 25-57.
47. Decker, D. S. (1998) Econ. Bot. 42, 4-15.
48. Allaby, R. G. & Brown, T. A. (2003) Genome 46, 448-453. [PubMed]
49. Salamini, F., Heun, M., Brandolini, A., Özkan, H. & Wunder, J. (2004) Genome 47, 615-620. [PubMed]
50. Diamond, J. (1997) Science 278, 1243-1244.
51. Kato Y., T. A. (1984) Evol. Biol. 17, 219-253.
52. Galinat, W. C. (1988) in Corn and Corn Improvement, eds. Sprague, G. F. & Dudley, J. W. (Am. Soc. Agronomy/Crop Sci. Soc. Am., Madison, WI), pp. 1-31.
53. Knapp, S., Bohs, L., Nee, M. & Spooner, D. M. (2004) Comp. Funct. Genomics 5, 285-291. [PMC free article] [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...