Taming the wild: resolving the gene pools of non-model Arabidopsis lineages
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25344686
PubMed Central
PMC4216345
DOI
10.1186/s12862-014-0224-x
PII: s12862-014-0224-x
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis klasifikace cytologie genetika MeSH
- biologická evoluce MeSH
- chloroplasty genetika MeSH
- ekotyp MeSH
- fylogeografie MeSH
- genetická variace MeSH
- genom chloroplastový MeSH
- genový pool MeSH
- mikrosatelitní repetice MeSH
- tok genů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: Wild relatives in the genus Arabidopsis are recognized as useful model systems to study traits and evolutionary processes in outcrossing species, which are often difficult or even impossible to investigate in the selfing and annual Arabidopsis thaliana. However, Arabidopsis as a genus is littered with sub-species and ecotypes which make realizing the potential of these non-model Arabidopsis lineages problematic. There are relatively few evolutionary studies which comprehensively characterize the gene pools across all of the Arabidopsis supra-groups and hypothesized evolutionary lineages and none include sampling at a world-wide scale. Here we explore the gene pools of these various taxa using various molecular markers and cytological analyses. RESULTS: Based on ITS, microsatellite, chloroplast and nuclear DNA content data we demonstrate the presence of three major evolutionary groups broadly characterized as A. lyrata group, A. halleri group and A. arenosa group. All are composed of further species and sub-species forming larger aggregates. Depending on the resolution of the marker, a few closely related taxa such as A. pedemontana, A. cebennensis and A. croatica are also clearly distinct evolutionary lineages. ITS sequences and a population-based screen based on microsatellites were highly concordant. The major gene pools identified by ITS sequences were also significantly differentiated by their homoploid nuclear DNA content estimated by flow cytometry. The chloroplast genome provided less resolution than the nuclear data, and it remains unclear whether the extensive haplotype sharing apparent between taxa results from gene flow or incomplete lineage sorting in this relatively young group of species with Pleistocene origins. CONCLUSIONS: Our study provides a comprehensive overview of the genetic variation within and among the various taxa of the genus Arabidopsis. The resolved gene pools and evolutionary lineages will set the framework for future comparative studies on genetic diversity. Extensive population-based phylogeographic studies will also be required, however, in particular for A. arenosa and their affiliated taxa and cytotypes.
Centre for Organismal Studies Heidelberg Heidelberg University Heidelberg 69120 Germany
Department of Life Sciences Cheng Kung University Tainan Taiwan
Institute of Botany Academy of Sciences of the Czech Republic Průhonice CZ 25243 Czech Republic
Institute of Botany Slovak Academy of Sciences Dúbravská cesta 9 Bratislava SK 845 23 Slovakia
Zobrazit více v PubMed
Clauss M, Koch MA. Arabidopsis and its poorly known relatives. Trends Pl Sci. 2006;11:449–459. doi: 10.1016/j.tplants.2006.07.005. PubMed DOI
Al-Shehbaz IA, O’Kane SL, Price RA. Generic placement of species excluded from Arabidopsis. Novon. 1999;9:296–307. doi: 10.2307/3391724. DOI
Al-Shehbaz IA, O’Kane SL: Taxonomy and phylogeny ofArabidopsis(Brassicaceae). In The Arabidopsis Book 2002, Volume 1. Edited by Torii K. The American Society of Plant Biologists; 2002:e0001. doi:10.1199/tab.0001. PubMed PMC
Koch M, Bishop J, Mitchell-Olds T. Molecular systematics and evolution of Arabidopsis and Arabis. Pl Biol. 1999;1:529–537. doi: 10.1111/j.1438-8677.1999.tb00779.x. DOI
Koch MA, Haubold B, Mitchell-Olds T. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae) Mol Biol Evol. 2000;17:1483–1498. doi: 10.1093/oxfordjournals.molbev.a026248. PubMed DOI
Koch MA, Haubold B, Mitchell-Olds T. Molecular systematics of the Brassicaceae: evidence from coding plastidic MATK and nuclear CHS sequences. Am J Bot. 2001;88:534–544. doi: 10.2307/2657117. PubMed DOI
Karl R, Koch MA. A world-wide perspective on crucifer speciation and evolution: phylogeny, biogeography and trait evolution in tribe Arabideae. Ann Bot. 2013;112:983–1001. doi: 10.1093/aob/mct165. PubMed DOI PMC
O’Kane SL, Al-Shehbaz IA. A synopsis of Arabidopsis (Brassicaceae) Novon. 1997;7:323–327. doi: 10.2307/3391949. DOI
O’Kane SL, Al-Shehbaz IA. Phylogenetic position and generic limits of Arabidopsis (Brassicaceae) based on sequences of nuclear ribosomal DNA. Ann Missouri Bot Gard. 2003;90:603–612. doi: 10.2307/3298545. DOI
Warwick SI, Al-Shehbaz IA, Sauder CA. Phylogenetic position of Arabis arenicola and generic limits of Aphragmus and Eutrema (Brassicaceae) based on sequences of nuclear ribosomal DNA. Can J Bot. 2006;84:269–281. doi: 10.1139/b05-161. DOI
Kadota Y. Arabidopsis umezawana (Brassicaceae), a new species from Mt. Rishirizan, Rishiri Island, Hokkaido, Northern Japan. J Jpn Bot. 2007;82:232–237.
Dorofeyev VI. Cruciferae of European Russia. Turczaninowia. 2002;5:5–114.
Marhold K, Perný M, Kolník M. Miscellaneous validations in Cruciferae and Crassulaceae. Willdenowia. 2003;33:69–70.
Shimizu KK, Fujii S, Marhold K, Watanabe K, Kudoh H. Arabidopsis kamchatica (Fisch. ex DC.) K. Shimizu & Kudoh and A. kamchatica subsp. kawasakiana (Makino) K. Shimizu & Kudoh, new combinations. Acta Phytotax Geobot. 2005;56:163–172.
Kolnik M, Marhold K. Distribution, chromosome numbers and nomenclature conspect of Arabidopsis halleri (Brassicaceae) in theCarpathians. Biologia (Bratislava) 2006;61:41–50. doi: 10.2478/s11756-006-0007-y. DOI
Iljinska A, Didukh Y, Burda R, Korotschenko I. Ecoflora of Ukraine. Kyiv: Phytosociocentre Press; 2007.
Elven DR, Murray J. New combinations in the Panarctic vascular plant flora. J Bot Res Inst Texas. 2008;2:433–438.
Koch MA, Wernisch M, Schmickl R. Arabidopsis thaliana’s wild relatives: an updated overview on systematics, taxonomy and evolution. Taxon. 2008;57:933–943.
Schmickl R, Paule J, Klein J, Marhold K, Koch MA. The evolutionary history of the Arabidopsis arenosa species complex: Highly diverse tetraploids mask that the Western Carpathians are the center of species and genetic diversity. PLoS One. 2012;7:e42691. doi: 10.1371/journal.pone.0042691. PubMed DOI PMC
Koch MA, Kiefer M, German D, Al-Shehbaz IA, Franzke A, Mummenhoff K. BrassiBase: tools and biological resources to study characters and traits in the Brassicaceae – version 1.1. TAXON. 2012;61:1001–1009.
Koch MA, German D. Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Frontiers Pl Science. 2013;4:e267. PubMed PMC
Koch MA, Matschinger M. Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2007;104:6272–6277. doi: 10.1073/pnas.0701338104. PubMed DOI PMC
Castric V, Bechsgaard J, Schierup MH, Vekemans X. Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet. 2008;4:e1000168. doi: 10.1371/journal.pgen.1000168. PubMed DOI PMC
Säll T, Jakobsson M, Lind-Halldén C, Halldén C. Chloroplast DNA indicates a single origin of the allotetraploid Arabidopsis suecica. J Evol Biol. 2003;16:1019–1029. doi: 10.1046/j.1420-9101.2003.00554.x. PubMed DOI
Jakobsson M, Hagenblad J, Tavaré S, Säll T, Halldén C, Lind-Halldén C, Nordborg M. A unique recent origin of the allotetraploid species Arabidopsis suecica: evidence from nuclear DNA markers. Mol Biol Evol. 2006;23:1217–1231. doi: 10.1093/molbev/msk006. PubMed DOI
Schmickl R, Jørgensen MH, Brysting AK, Koch MA. Phylogeographic implications for the North American boreal-arctic Arabidopsis lyrata complex. Plant Ecol Div. 2008;1:245–254. doi: 10.1080/17550870802349138. DOI
Schmickl R, Jorgenson M, Brysting A, Koch MA. The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evol Biol. 2010;10:e98. doi: 10.1186/1471-2148-10-98. PubMed DOI PMC
Shimizu-Inatsugi R, Lihová J, Iwanaga H, Kudoh H, Marhold K, Savolainen O, Watanabe K, Yakubov VV, Shimizu KK. The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Mol Ecol. 2009;18:4024–4048. doi: 10.1111/j.1365-294X.2009.04329.x. PubMed DOI
Schmickl R, Koch MA. Arabidopsis hybrid speciation processes. Proc Natl Acad Sci U S A. 2011;108:14192–14197. doi: 10.1073/pnas.1104212108. PubMed DOI PMC
Pauwels M, Saumitou-Laprade P, Holl AC, Petit D, Bonnin I. Multiple origin of metallicolous populations of the pseudometallophyte Arabidopsis halleri (Brassicaceae) in Central Europe: the cpDNA testimony. Molec Ecol. 2005;14:4403–4414. doi: 10.1111/j.1365-294X.2005.02739.x. PubMed DOI
Pauwels M, Vekemans X, Godé C, Frérot H, Castric V, Saimitou-Laprade P. Nuclear and chloroplast DNA phy logeography reveals vicariance among European popula tions of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae) New Phytol. 2012;193:916–928. doi: 10.1111/j.1469-8137.2011.04003.x. PubMed DOI
Tedder A, Hoebe PN, Ansell SK, Mable BK. Using chloroplast genes for phylogeography in Arabidopsis lyrata. Diversity. 2010;2:653–678. doi: 10.3390/d2040653. DOI
Hoebe PN, Stift M, Tedder A, Mable BK. Multiple losses of self-incompatibility in North-American Arabidopsis lyrata? Phylogeographic context and population genetic consequences. Mol Ecol. 2009;18:4294–4939. doi: 10.1111/j.1365-294X.2009.04400.x. PubMed DOI
Clauss M, Mitchell-Olds T. Population genetic structure of Arabidopsis lyrata in Europe. Mol Ecol. 2006;15:2753–2766. doi: 10.1111/j.1365-294X.2006.02973.x. PubMed DOI
Kuittinen H, Niittyvuopio A, Rinne P, Savolainen O. Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism. Mol Biol Evol. 2008;25:319–329. doi: 10.1093/molbev/msm257. PubMed DOI
Muller MH, Leppälä J, Savolainen O. Genome-wide effects of postglacial colonization in Arabidopsis lyrata. Heredity. 2008;100:47–58. doi: 10.1038/sj.hdy.6801057. PubMed DOI
Riihimäki M, Podolsky R, Kuittinen H, Koelewijn H, Savolainen O. Studying genetics of adaptive variation in model organisms: flowering time variation in Arabidopsis lyrata. Genetica. 2005;123:63–74. doi: 10.1007/s10709-003-2711-7. PubMed DOI
Leinonen PH, Sandring S, Quilot B, Clauss MJ, Mitchell-Olds T, Agren J, Savolainen O. Local adaptation in European populations of Arabidopsis lyrata (Brassicaceae) Am J Bot. 2009;96:1129–1137. doi: 10.3732/ajb.0800080. PubMed DOI
Turner TL, Von Wettberg EJ, Nuzhdin SV. Genomic analysis of differentiation between soil types reveals candidate genes for local adaptation in Arabidopsis lyrata. PLoS One. 2008;3:e3183. doi: 10.1371/journal.pone.0003183. PubMed DOI PMC
Savolainen O, Kuittinen H: Arabidopsis lyratagenetics. In Genetics and Genomics of the Brassicaceae. Edited by Bancroft I, Schmidt R. New York: Springer Verlag; 2011:347–372.
Comai L, Tyagi AP, Winter K, Holmes-Davis R, Reynolds SH, Stevens Y, Byers B. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell. 2000;12:1551–1568. doi: 10.1105/tpc.12.9.1551. PubMed DOI PMC
Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L. Genomic changes in synthetic Arabidopsis polyploids. Plant J. 2005;41:221–230. doi: 10.1111/j.1365-313X.2004.02297.x. PubMed DOI
Hollister J, Arnold B, Svedin E, Xue K, Dilkes B, Bomblies K. Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 2012;8:e1003093. doi: 10.1371/journal.pgen.1003093. PubMed DOI PMC
Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD, Franklin FCH, Bomblies K. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol. 2013;23:2151–2156. doi: 10.1016/j.cub.2013.08.059. PubMed DOI PMC
Hunter B, Bomblies K: Progress and promise in usingArabidopsisto study adaptation, divergence and speciation. In The Arabidopsis Book 2010, Volume 8. Edited by Torii K. Rockville, MD: American Society of Plant Biologists; 2010:e0138. PubMed PMC
Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, Haberer G, Hollister JD, Ossowski S, Ottilar RP, Salamov AA, Schneeberger K, Spannagl M, Wang X, Nasrallah ME, Bergelson J, Carrington JC, Gaut BS, Schmutz J, Mayer KFX, Van de Peer Y, Grigoriev IV, Nordborg M, Weigel D, Guo YL. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 2011;43:476–481. doi: 10.1038/ng.807. PubMed DOI PMC
Koch M, Dobes C, Mitchell-Olds T. Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae) Mol Biol Evol. 2003;20:338–350. doi: 10.1093/molbev/msg046. PubMed DOI
Jorgensen MH, Ehrich D, Schmickl R, Koch MA, Brysting A. Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae) BMC Evol Biol. 2011;11:e346. doi: 10.1186/1471-2148-11-346. PubMed DOI PMC
Ross-Ibarra J, Wright SI, Foxe JP, Kawabe A, DeRose-Wilson L, Gos G, Charlesworth D, Gaut BS. Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS One. 2008;3:e2411. doi: 10.1371/journal.pone.0002411. PubMed DOI PMC
Mable BK, Schierup MH, Charlesworth D. Estimating the number, frequency, and dominance of S-alleles in a natural population of Arabidopsis lyrata (Brassicaceae) with sporophytic control of self-incompatibility. Heredity. 2003;90:422–431. doi: 10.1038/sj.hdy.6800261. PubMed DOI
Mable BK, Robertson AV, Dart S, DiBerardo C, Witham L. Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences. Evolution. 2005;59:1437–1448. doi: 10.1111/j.0014-3820.2005.tb01794.x. PubMed DOI
Roux C, Pauwels M, Ruggiero MV, Charlesworth D, Castric V, Vekemans X. Recent and ancient signature of balancing selection around the S-locus in Arabidopsis halleri and Arabidopsis lyrata. Mol Biol Evol. 2013;30:435–447. doi: 10.1093/molbev/mss246. PubMed DOI PMC
Měsíček J. Chromosome counts in Cardaminopsis arenosa agg. (Cruciferae) Preslia. 1970;42:225–248.
Tsuchimatsu T, Kaiser P, Yew CL, Bachelier JB, Shimizu KK. Recent loss of self-incompatibility by degradation of the male component in allotetraploid Arabidopsis kamchatica. PLoS Genet. 2012;8:e1002838. doi: 10.1371/journal.pgen.1002838. PubMed DOI PMC
Koch M, Mummenhoff K, Hurka H. Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe: evidence from genetic studies based on isozyme analysis. Biochem Syst Ecol. 1998;26:823–838. doi: 10.1016/S0305-1978(98)00057-X. DOI
Roux C, Castric V, Pauwels M, Wright SI, Saumitou-Laprade P, Vekemans X. Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS One. 2011;6:e26872. doi: 10.1371/journal.pone.0026872. PubMed DOI PMC
Hayek A: Flora von Steiermark. Berlin: Verlag von Gebrüder Bornträger; 1908–1914
Měsíček J. Cardaminopsis. In: Marhold K, Hindák F, editors. Zoznam nižších a vyšších rastlín Slovenska – Checklist of non-vascular and vascular plants of Slovakia. Bratislava: VEDA; 1998. pp. 395–396.
Kolník M. Arabidopsis. In: Marhold K, Mártonfi P, Mereda P Jr, Mráz P, editors. Chromosome number Survey of The Ferns and Flowering Plants of Slovakia. Bratislava: VEDA; 2012. pp. 94–102.
Jakobsson M, Hagenblad J, Tavaré S, Säll T, Halldén C, Lind-Halldén C, Nordborg M. A unique recent origin of the allotetraploid species Arabidopsis suecica: evidence from nuclear DNA markers. Molec Biol Evol. 2006;23:1217–1231. doi: 10.1093/molbev/msk006. PubMed DOI
Schmuths H, Meister A, Horres R, Bachmann K. Genome size variation among accessions of Arabidopsis thaliana. Ann Bot. 2004;93:317–321. doi: 10.1093/aob/mch037. PubMed DOI PMC
Johnston SP, Pepper AE, Hall AE, Chen ZF, Hodnett G, Drabek J, Lopez R, Price HJ. Evolution of genome size in Brassicaceae. Ann Bot. 2005;95:229–235. doi: 10.1093/aob/mci016. PubMed DOI PMC
Lysak MA, Koch MA, Leitch IJ, Beaulieau JM, Meister A. The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol. 2009;26:85–98. doi: 10.1093/molbev/msn223. PubMed DOI
Wolf DE, Steets JA, Houliston GJ, Takebayashi N: Genome size variation and evolution in a allotetraploidArabidopsis kamchaticaand its parents,Arabidopsis lyrataandArabidopsis halleri.AoB PLANTS 2014, 6: doi:10.1093/aobpla/plu025. PubMed PMC
Dart S, Kron P, Mable BK. Characterizing polyploidy in Arabidopsis lyrata using chromosome counts and flow cytometry. Canad J Bot. 2004;82:185–197. doi: 10.1139/b03-134. DOI
Jørgensen MH, Ehrich D, Schmickl R, Koch MA, Brysting AK. Interspecific and interploidal gene flow in central european Arabidopsis (Brassicaceae) BMC Evol Biol. 2011;11:e346. doi: 10.1186/1471-2148-11-346. PubMed DOI PMC
Al-Shebaz IA. Flora of North America. Oxford: Oxford University Press; 2010. Arabidopsis; pp. 447–449.
Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 1987;19:11–15.
Dobeš CH, Mitchell-Olds T, Koch MA. Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. x divaricarpa, and A. holboellii (Brassicaceae) Mol Ecol. 2004;13:349–370. doi: 10.1046/j.1365-294X.2003.02064.x. PubMed DOI
Dobes C, Mitchell-Olds T, Koch M. Intraspecific diversification in North American Arabis drummondii, A. ×divaricarpa, and A. holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers – an integrative approach. Am J Bot. 2004;91:2087–2101. doi: 10.3732/ajb.91.12.2087. PubMed DOI
Clauss MJ, Cobban H, Mitchell-Olds T. Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaeae) Mol Ecol. 2002;11:591–601. doi: 10.1046/j.0962-1083.2002.01465.x. PubMed DOI
Doležel J, Greilhuber J, Suda J. Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc. 2007;2:2233–2244. doi: 10.1038/nprot.2007.310. PubMed DOI
Temsch EM, Greilhuber J, Krisai R. Genome size in liverworts. Preslia. 2010;82:63–80.
Doležel J, Bartoš J. Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot. 2005;95:99–110. doi: 10.1093/aob/mci005. PubMed DOI PMC
R Development Core Team . R: A language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
Dolezel J, Sgorbati S, Lucretti S. Comparison of three fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol Plantarum. 1992;85:625–631. doi: 10.1111/j.1399-3054.1992.tb04764.x. DOI
Kiefer M, Schmickl R, German D, Lysak M, Al-Shehbaz IA, Franzke A, Mummenhoff K, Stamatakis A, Koch MA. BrassiBase: introduction to a novel knowledge database on Brassicaceae evolution. Plant Cell Physiol. 2014;55:e3. doi: 10.1093/pcp/pct158. PubMed DOI
Koch MA, Dobeš C, Matschinger M, Bleeker W, Vogel J, Kiefer M, Mitchell-Olds T. Evolution of the trnF(GAA) gene in Arabidopsis relatives and the Brassicaceae family: monophyletic origin and subsequent diversification of a plastidic pseudogene. Mol Biol Evol. 2005;22:1032–1043. doi: 10.1093/molbev/msi092. PubMed DOI
Dobeš C, Kiefer C, Kiefer M, Koch MA. Plastidic trnFUUC pseudogenes in North American genus Boechera (Brassicaceae): mechanistic aspects of evolution. Plant Biol. 2007;9:502–515. doi: 10.1055/s-2006-955978. PubMed DOI
Koch MA, Dobeš C, Kiefer C, Schmickl R, Klimeš L, Lysak MA. Supernetwork identifies multiple events of plastid trnF(GAA) pseudogene evolution in the Brassicaceae. Mol Biol Evol. 2007;24:63–73. doi: 10.1093/molbev/msl130. PubMed DOI
Schmickl R, Kiefer C, Dobeš C, Koch MA: Evolution oftrnF(GAA) pseudogenes in cruciferous plants.Plant Syst Evol 2008, [doi:10.1007/s00606-008-0030-2]
Müller K, Quandt D, Müller J, Neinhuis C. PhyDE, Version 0.92: Phylogenetic Data Editor. 2005.
Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x. PubMed DOI
Templeton AR, Crandall KA, Sing CF. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics. 1992;132:619–633. PubMed PMC
Stamatakis A: RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies.Bioinformatics 2014, doi:10.1093/bioinformatics/btu033. PubMed PMC
Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sunderland, MA: Sinauer Associates; 2002.
Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:254–267. doi: 10.1093/molbev/msj030. PubMed DOI
Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Eco Res. 2010;10:564–567. doi: 10.1111/j.1755-0998.2010.02847.x. PubMed DOI
Nei M. Molecular Evolutionary Genetics. New York: Columbia University Press; 1987.
Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC
Hubisz M, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Molec Ecol Res. 2009;9:1322–1332. doi: 10.1111/j.1755-0998.2009.02591.x. PubMed DOI PMC
Ehrich D. AFLPdat: a collection of R functions for convenient handling of AFLP data. Mol Ecol Notes. 2006;6:603–604. doi: 10.1111/j.1471-8286.2006.01380.x. DOI
Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW. Genetic structure of human populations. Science. 2002;298:2381–2385. doi: 10.1126/science.1078311. PubMed DOI
Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol. 2005;14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI
Earl DA, vonHoldt BM. Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Cons Genet Res. 2012;4:359–361. doi: 10.1007/s12686-011-9548-7. DOI
Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23:1801–1806. doi: 10.1093/bioinformatics/btm233. PubMed DOI
Rosenberg NA. Documentation for Distruct Software: Version 1.1. Michigan: University of Michigan; 2007.
Mable BK, Beland J, Di Berardo C. Inheritance and dominance of self-incompatibility alleles in polyploid Arabidopsis lyrata. Heredity. 2004;93:476–486. doi: 10.1038/sj.hdy.6800526. PubMed DOI
Säll T, Lind-Halldén C, Jakobsson M, Halldén C. Mode of reproduction in Arabidopsis suecica. Hereditas. 2004;141:313–317. doi: 10.1111/j.1601-5223.2004.01833.x. PubMed DOI
Complex Polyploids: Origins, Genomic Composition, and Role of Introgressed Alleles
A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History