Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Cryptic genetic diversity in Solanum elaeagnifolium (Solanaceae) from South America

Franco E. Chiarini A , Marisel A. Scaldaferro A B , Gabriel Bernardello A B and M. Cristina Acosta A B C
+ Author Affiliations
- Author Affiliations

A Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET-Universidad Nacional de Córdoba, Argentina.

B Facultad de Ciencias Exactas, Físicas y Naturales (Universidad Nacional de Córdoba), Argentina.

C Corresponding author. Email: mcacosta@imbiv.unc.edu.ar

Australian Journal of Botany 66(7) 531-540 https://doi.org/10.1071/BT17245
Submitted: 12 December 2017  Accepted: 19 October 2018   Published: 21 November 2018

Abstract

Solanum elaeagnifolium is a global invasive weed that is polyploid in the South American range. Our aim was to establish the origin and distribution of these polyploid lineages, together with their relationship with the invasion of new habitats. Ploidy level was determined in 26 natural populations using chromosomal counts, and two non-coding plastid regions trnL-trnF and rpl32F-trnL were sequenced. Relationships among haplotypes were examined by a median-joining network, and groups of populations were identified by employing a spatial analysis of molecular variance. Phylogenetic relationships among haplotypes were reconstructed using Bayesian inference, and divergence times were estimated using BEAST. We found 21 haplotypes structured into three lineages: one with diploids in North America and invaded areas, and two in South America that developed independent polyploidisation events. The separation of lineages took place during the Pliocene with more recent divergences in the Early Pleistocene. The existence of three lineages can be attributed to the uplift of the Andes and the emergence of the Isthmus of Panama. Diversification within each lineage may be related to the recent cyclical glacial variation throughout the Pleistocene creating haplotype diversity and recurrent polyploidy. Thus, the South American populations of S. elaeagnifolium did not originate from a recent colonisation but are established ancient lineages.

Additional keywords: geological events, haplotypes, invasion, polyploidy, silverleaf nightshade, Solanum elaeagnifolium, weed.


References

Ainouche ML, Baumel A, Salmon A (2004) Spartina anglica C.E. Hubbard: a natural model system for studying early evolutionary changes that affect allopolyploid genomes. Biological Journal of the Linnean Society. Linnean Society of London 82, 475–484.
Spartina anglica C.E. Hubbard: a natural model system for studying early evolutionary changes that affect allopolyploid genomes.Crossref | GoogleScholarGoogle Scholar |

Albach DC (2007) Amplified fragment length polymorphisms and sequence data in the phylogenetic analysis of polyploids: multiple origins of Veronica cymbalaria (Plantaginaceae). New Phytologist 176, 481–498.
Amplified fragment length polymorphisms and sequence data in the phylogenetic analysis of polyploids: multiple origins of Veronica cymbalaria (Plantaginaceae).Crossref | GoogleScholarGoogle Scholar |

Avise JC (2000) ‘Phylogeography: the history and formation of species.’ (Harvard University Press: Cambridge, UK)

Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.
Median-joining networks for inferring intraspecific phylogenies.Crossref | GoogleScholarGoogle Scholar |

Boukhris-Bouhachem S, Hullé M, Rouzé-Jouan J, Glais L, Kerlan C (2007) Solanum elaeagnifolium, a potential source of Potato virus Y (PVY) propagation. Bulletin OEPP. EPPO Bulletin. European and Mediterranean Plant Protection Organisation 37, 125–128.
Solanum elaeagnifolium, a potential source of Potato virus Y (PVY) propagation.Crossref | GoogleScholarGoogle Scholar |

Bowen CC (1956) Freezing by liquid carbon dioxide in making slides permanent. Stain Technology 31, 87–90.
Freezing by liquid carbon dioxide in making slides permanent.Crossref | GoogleScholarGoogle Scholar |

Boyd JW, Murray DS, Tyrl RJ (1984) Silverleaf nightshade, Solanum elaeagnifolium, origin, distribution and relation to man. Economic Botany 38, 210–217.
Silverleaf nightshade, Solanum elaeagnifolium, origin, distribution and relation to man.Crossref | GoogleScholarGoogle Scholar |

Brochmann C, Brysting AK (2008) The Arctic – an evolutionary freezer? Plant Ecology & Diversity 1, 181–195.
The Arctic – an evolutionary freezer?Crossref | GoogleScholarGoogle Scholar |

Brown JH (1984) On the relationship between abundance and distribution of species. American Naturalist 124, 255–279.
On the relationship between abundance and distribution of species.Crossref | GoogleScholarGoogle Scholar |

Burnier J, Buerki S, Arrigo N, Küpfer P, Alvarez N (2009) Genetic structure and evolution of Alpine polyploid complexes: Ranunculus kuepferi (Ranunculaceae) as a case study. Molecular Ecology 18, 3730–3744.
Genetic structure and evolution of Alpine polyploid complexes: Ranunculus kuepferi (Ranunculaceae) as a case study.Crossref | GoogleScholarGoogle Scholar |

Catalano SA, Vilardi JC, Tosto D, Saidman BO (2008) Molecular phylogeny and diversification history of Prosopis (Fabaceae: Mimosoideae). Biological Journal of the Linnean Society. Linnean Society of London 93, 621–640.
Molecular phylogeny and diversification history of Prosopis (Fabaceae: Mimosoideae).Crossref | GoogleScholarGoogle Scholar |

Chiarini FE (2014) Variation in rDNA loci of polyploid Solanum elaeagnifolium (Solanaceae). New Zealand Journal of Botany 52, 277–284.
Variation in rDNA loci of polyploid Solanum elaeagnifolium (Solanaceae).Crossref | GoogleScholarGoogle Scholar |

Chiarini F, Barboza GE (2007) Placentation patterns and seed number in fruits of South American Solanum subgen. Leptostemonum (Solanaceae) species. Darwiniana 45, 163–174.

Christodoulakis NS, Lampri PN, Fasseas C (2009) Structural and cytochemical investigation of the leaf of silverleaf nightshade (Solanum elaeagnifolium), a drought-resistant alien weed of the Greek flora. Australian Journal of Botany 57, 432–438.
Structural and cytochemical investigation of the leaf of silverleaf nightshade (Solanum elaeagnifolium), a drought-resistant alien weed of the Greek flora.Crossref | GoogleScholarGoogle Scholar |

Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134, 959–969.

Deng B, Du W, Liu C, Sun W, Tian S, Dong H (2012) Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids? Plant Growth Regulation 66, 37–47.
Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids?Crossref | GoogleScholarGoogle Scholar |

Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar |

Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571
A simulated annealing approach to define the genetic structure of populations.Crossref | GoogleScholarGoogle Scholar |

Feuerherdt L (2009) Overcoming a deep rooted perennial problem – silverleaf nightshade (Solanum elaeagnifolium) in South Australia. Plant Protection Quarterly 24, 123–124.

Flatscher R, García PE, Hülber K, Sonnleitner M, Winkler M, Saukel J, Schneeweiss GM, Schönswetter P (2015) Underestimated diversity in one of the world’s best studied mountain ranges: the polyploid complex of Senecio carniolicus (Asteraceae) contains four species in the European Alps. Phytotaxa 213, 1–21.
Underestimated diversity in one of the world’s best studied mountain ranges: the polyploid complex of Senecio carniolicus (Asteraceae) contains four species in the European Alps.Crossref | GoogleScholarGoogle Scholar |

Goeden RD (1971) Insect ecology of silverleaf nightshade. Weed Science 19, 45–51.

Gopurenko D, Wang A, Zhu X, Lepschi BJ, Wu H (2014) Origins and diversity of exotic silverleaf nightshade (Solanum elaeagnifolium) present in Australia as determined by sequence analysis of a chloroplast intergenic spacer region. In ‘Proceedings of the 19th Australasian Weeds Conference’. (Ed. M Baker) pp. 392–395 (Tasmanian Weed Society: Hobart, Tas.)

Guerra M (1983) O uso da Giemsa na citogenética vegetal. Ciencia e Cultura 35, 190–193.

Hewitt GM (2001) Speciation, hybrid zones and phylogeography – or seeing genes in space and time. Molecular Ecology 10, 537–549.
Speciation, hybrid zones and phylogeography – or seeing genes in space and time.Crossref | GoogleScholarGoogle Scholar |

Hoorn C, Wesselingh FP, Ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927–931.
Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity.Crossref | GoogleScholarGoogle Scholar |

Hörandl E, Paun O, Johansson JT, Lehnebach C, Armstrong T, Chen L, Lockhart P (2005) Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Molecular Phylogenetics and Evolution 36, 305–327.
Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis.Crossref | GoogleScholarGoogle Scholar |

Ilçim A, Behçet L (2007) Solanum elaeagnifolium Cav. in Turkey. Turkish Journal of Botany 31, 577–579.

Jong K (1997) ‘Laboratory manual of plant cytological techniques.’ (Royal Botanic Garden: Edinburgh, UK)

Jordon-Thaden I, Koch M (2008) Species richness and polyploid patterns in the genus Draba (Brassicaceae): a first global perspective. Plant Ecology & Diversity 1, 255–263.
Species richness and polyploid patterns in the genus Draba (Brassicaceae): a first global perspective.Crossref | GoogleScholarGoogle Scholar |

Knapp S, Sagona E, Carbonell AKZ, Chiarini F (2017) A revision of the Solanum elaeagnifolium clade (Elaeagnifolium clade; subgenus Leptostemonum, Solanaceae). PhytoKeys 84, 1–104.
A revision of the Solanum elaeagnifolium clade (Elaeagnifolium clade; subgenus Leptostemonum, Solanaceae).Crossref | GoogleScholarGoogle Scholar |

Kochert G, Stocker HT, Gimenes M, Galgaro L, Lopes CR, Moore K (1996) RFLP and cytogenetic evidence on the origin and evolution of allotetraploid domesticated peanut, Arachis hypogea (Leguminosae). American Journal of Botany 83, 1282–1291.
RFLP and cytogenetic evidence on the origin and evolution of allotetraploid domesticated peanut, Arachis hypogea (Leguminosae).Crossref | GoogleScholarGoogle Scholar |

Levin DA (2004) Ecological speciation: the role of disturbance. Systematic Botany 29, 225–233.
Ecological speciation: the role of disturbance.Crossref | GoogleScholarGoogle Scholar |

Levin RA, Myers NR, Bohs L (2006) Phylogenetic relationships among the ‘spiny solanums’ (Solanum subgenus Leptostemonum, Solanaceae). American Journal of Botany 93, 157–169.
Phylogenetic relationships among the ‘spiny solanums’ (Solanum subgenus Leptostemonum, Solanaceae).Crossref | GoogleScholarGoogle Scholar |

Matzke MA, Matzke AJM (1998) Polyploidy and transposons. Trends in Ecology & Evolution 13, 241
Polyploidy and transposons.Crossref | GoogleScholarGoogle Scholar |

Mekki M (2007) Biology, distribution and impacts of silverleaf nightshade (Solanum elaeagnifolium Cav.). Bulletin OEPP. EPPO Bulletin. European and Mediterranean Plant Protection Organisation 37, 114–118.
Biology, distribution and impacts of silverleaf nightshade (Solanum elaeagnifolium Cav.).Crossref | GoogleScholarGoogle Scholar |

Miller JS, Venable DL (2000) Polyploidy and the evolution of gender dimorphism in plants. Science 289, 2335–2338.
Polyploidy and the evolution of gender dimorphism in plants.Crossref | GoogleScholarGoogle Scholar |

Moore AJ, Valtueña FJ, Dillenberger MS, Kadereit JW, Preston CD (2017) Intraspecific haplotype diversity in Cherleria sedoides L. (Caryophyllaceae) is best explained by chloroplast capture from an extinct species. Alpine Botany 1–13.
Intraspecific haplotype diversity in Cherleria sedoides L. (Caryophyllaceae) is best explained by chloroplast capture from an extinct species.Crossref | GoogleScholarGoogle Scholar |

Nylander JA (2004) ‘MrModelTest.’ (Evolutionary Biology Centre, Uppsala University: Uppsala, Sweden)

Ortiz-Jaureguizar E, Cladera GA (2006) Paleoenvironmental evolution of southern South America during the Cenozoic. Journal of Arid Environments 66, 498–532.
Paleoenvironmental evolution of southern South America during the Cenozoic.Crossref | GoogleScholarGoogle Scholar |

Peirson JA, Dick CW, Reznicek AA (2013) Phylogeography and polyploid evolution of North American goldenrods (Solidago subsect. Humiles, Asteraceae). Journal of Biogeography 40, 1887–1898.

Pound GE, Cox SJ, Doncaster CP (2004) The accumulation of deleterious mutations within the frozen niche variation hypothesis. Journal of Evolutionary Biology 17, 651–662.
The accumulation of deleterious mutations within the frozen niche variation hypothesis.Crossref | GoogleScholarGoogle Scholar |

Rabassa J, Coronato A (2009) Glaciations in Patagonia and Tierra del Fuego during the Ensenadan Stage/Age (Early Pleistocene–earliest Middle Pleistocene). Quaternary International 210, 18–36.
Glaciations in Patagonia and Tierra del Fuego during the Ensenadan Stage/Age (Early Pleistocene–earliest Middle Pleistocene).Crossref | GoogleScholarGoogle Scholar |

Rebernig CA, Weiss-Schneeweiss H, Schneeweiss GM, Schönswetter P, Obermayer R, Villaseñor JL, Stuessy TF (2010) Quaternary range dynamics and polyploid evolution in an arid brushland plant species (Melampodium cinereum, Asteraceae). Molecular Phylogenetics and Evolution 54, 594–606.
Quaternary range dynamics and polyploid evolution in an arid brushland plant species (Melampodium cinereum, Asteraceae).Crossref | GoogleScholarGoogle Scholar |

Renny-Byfield S, Kovařík A, Chester M, Nichols RA, Macas J, Novák P, Leitch AR (2012) Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS One 7, e36963
Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar |

Särkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology 13, 214
A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree.Crossref | GoogleScholarGoogle Scholar |

Scaldaferro M, Chiarini F, Santiñaque F, Bernardello G, Moscone EA (2012) Geographical pattern and ploidy levels of the weed Solanum elaeagnifolium (Solanaceae) from Argentina. Genetic Resources and Crop Evolution 59, 1833–1847.
Geographical pattern and ploidy levels of the weed Solanum elaeagnifolium (Solanaceae) from Argentina.Crossref | GoogleScholarGoogle Scholar |

Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN: a software for population genetics data analysis, ver. 2.000. (Genetics and Biometry Laboratory, University of Geneva: Geneva, Switzerland). Available at: http://cmpg.unibe.ch/software/arlequin35/Arl35Downloads.html

Schönswetter P, Lachmayer M, Lettner C, Prehsler D, Rechnitzer S, Reich DS, Sonnleitner M, Wagner I, Hülber K, Schneeweiss GM, Trávníček P (2007) Sympatric diploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps are separated along an altitudinal gradient. Journal of Plant Research 120, 721–725.
Sympatric diploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps are separated along an altitudinal gradient.Crossref | GoogleScholarGoogle Scholar |

Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94, 275–288.
Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III.Crossref | GoogleScholarGoogle Scholar |

Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
Gaps as characters in sequence-based phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |

Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14, 348–352.
Polyploidy: recurrent formation and genome evolution.Crossref | GoogleScholarGoogle Scholar |

Soltis PS, Soltis DE (2000) The role of genetic and genomic changes in the success of polyploids. Proceedings of the National Academy of Sciences of the United States of America 97, 7051–7057.
The role of genetic and genomic changes in the success of polyploids.Crossref | GoogleScholarGoogle Scholar |

Soltis DE, Soltis PS, Pires JC, Kovařík A, Tate JA, Mavrodiev E (2004) Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biological Journal of the Linnean Society. Linnean Society of London 82, 485–501.
Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons.Crossref | GoogleScholarGoogle Scholar |

Soltis DE, Visger CJ, Soltis PS (2014) The polyploidy revolution then… and now: Stebbins revisited. American Journal of Botany 101, 1057–1078.
The polyploidy revolution then… and now: Stebbins revisited.Crossref | GoogleScholarGoogle Scholar |

Speranza PR, Seijo JG, Grela IA, Solís Neffa VG (2007) Chloroplast DNA variation in the Turnera sidoides L. complex (Turneraceae): biogeographical implications. Journal of Biogeography 34, 427–436.
Chloroplast DNA variation in the Turnera sidoides L. complex (Turneraceae): biogeographical implications.Crossref | GoogleScholarGoogle Scholar |

Stebbins GL (1985) Polyploidy, hybridization, and the invasion of new habitats. Annals of the Missouri Botanical Garden 72, 824–882.
Polyploidy, hybridization, and the invasion of new habitats.Crossref | GoogleScholarGoogle Scholar |

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis, version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis, version 6.0.Crossref | GoogleScholarGoogle Scholar |

te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany 109, 19–45.
The more the better? The role of polyploidy in facilitating plant invasions.Crossref | GoogleScholarGoogle Scholar |

Thompson JN, Nuismer SL, Merg K (2004) Plant polyploidy and the evolutionary ecology of plant/animal interactions. Biological Journal of the Linnean Society. Linnean Society of London 82, 511–519.
Plant polyploidy and the evolutionary ecology of plant/animal interactions.Crossref | GoogleScholarGoogle Scholar |

Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nature Reviews. Genetics 18, 411–424.
The evolutionary significance of polyploidy.Crossref | GoogleScholarGoogle Scholar |

Wahlert GA, Chiarini F, Bohs L (2014) Phylogeny of the Carolinense clade of Solanum (Solanaceae) inferred from nuclear and plastid DNA sequences. Systematic Botany 39, 1208–1216.
Phylogeny of the Carolinense clade of Solanum (Solanaceae) inferred from nuclear and plastid DNA sequences.Crossref | GoogleScholarGoogle Scholar |

Wendel JF (2000) Genome evolution in polyploids. Plant Molecular Biology 42, 225–249.
Genome evolution in polyploids.Crossref | GoogleScholarGoogle Scholar |

Whittemore AT, Olsen RT (2011) Ulmus americana (Ulmaceae) is a polyploid complex. American Journal of Botany 98, 754–760.
Ulmus americana (Ulmaceae) is a polyploid complex.Crossref | GoogleScholarGoogle Scholar |

Wilkie S (1997) Isolation of total genomic DNA. In ‘Plant molecular biology – a laboratory manual’. (Ed. MS Clark) pp. 3–15. (Springer-Verlag: Berlin, Germany)