Reticulate evolution is characterized by occasional hybridization between two species, creating a network of closely related taxa below and at the species level. In the present research, we aimed to verify the hypothesis of the allopolyploid origin of hexaploid C. album s. str., identify its putative parents and estimate the frequency of allopolyploidization events. We sampled 122 individuals of the C. album aggregate, covering most of its distribution range in Eurasia. Our samples included putative progenitors of C. album s. str. of both ploidy levels, i.e. diploids (C. ficifolium, C. suecicum) and tetraploids (C. striatiforme, C. strictum). To fulfil these objectives, we analysed sequence variation in the nrDNA ITS region and the rpl32-trnL intergenic spacer of cpDNA and performed genomic in-situ hybridization (GISH). Our study confirms the allohexaploid origin of C. album s. str. Analysis of cpDNA revealed tetraploids as the maternal species. In most accessions of hexaploid C. album s. str., ITS sequences were completely or nearly completely homogenized towards the tetraploid maternal ribotype; a tetraploid species therefore served as one genome donor. GISH revealed a strong hybridization signal on the same eighteen chromosomes of C. album s. str. with both diploid species C. ficifolium and C. suecicum. The second genome donor was therefore a diploid species. Moreover, some individuals with completely unhomogenized ITS sequences were found. Thus, hexaploid individuals of C. album s. str. with ITS sequences homogenized to different degrees may represent hybrids of different ages. This proves the existence of at least two different allopolyploid lineages, indicating a polyphyletic origin of C. album s. str.

Faculty of Environmental Sciences Czech University of Life Sciences Prague Kamýcká 129 CZ 165 21 Praha 6 Suchdol Czech Republic

Institute of Botany Czech Academy of Sciences Zámek 1 CZ 252 43 Průhonice Czech Republic

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Rieseberg LH, Willis JH. Plant speciation. Science. 2007; 317: 910–914. PubMed PMC

Lowe AJ, Abbott RJ. Origins of the new allopolyploid species

Kochert G, Stalker HT, Gimenes M, Galgaro L, Lopes CR, Moore K. RFLP and cytogenetic evidence on the origin and evolution of allotetraploid domesticated peanut,

Cook LM, Soltis PS, Brunsfeld SJ, Soltis DE. Multiple independent formations of

Segraves KA, Thompson JN, Soltis PS, Soltis DE. Multiple origins of polyploidy and the geographic structure of

Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, et al. Towards resolving the PubMed DOI PMC

Mandák B, Trávníček P, Paštová L, Kořínková D. Is hybridization involved in the evolution of the

Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PE, et al. Evolutionary genetics of genome merger and doubling in plants. Ann Rev Genet. 2008; 42: 443–461. 10.1146/annurev.genet.42.110807.091524 PubMed DOI

Leitch AR, Leitch IJ. Genomic plasticity and the diversity of polyploid plants. Science. 2008; 320: 481–483. 10.1126/science.1153585 PubMed DOI

Baack EJ, Rieseberg LH. A genomic view of introgression and hybrid speciation. Curr Oppin Genet Dev. 2007; 17: 513–518. PubMed PMC

Thompson JD, Lumaret E. The evolutionary dynamics of polyploid plants: origins, establishment and persistence. Trends Ecol Evol 1992; 7: 302–307. 10.1016/0169-5347(92)90228-4 PubMed DOI

Mandák B, Pyšek P, Lysák M, Suda J, Krahulcová A, Bímová K. Variation in DNA-ploidy levels of PubMed PMC

Mandák B, Pyšek P, Bímová K. History of the invasion and distribution of

Mandák B, Bímová K, Pyšek P, Štěpánek J, Plačková I. Isoenzyme diversity in

Soltis DE, Soltis PS. Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol. 1999; 14: 348–352. PubMed

Shimizu-Inatsugi R, Lihová J, Iwanaga H, Kudoh H, Marhold K, Savolainen O, et al. The allopolyploid PubMed DOI

Symonds VV, Soltis PS, Soltis DE. Dynamics of polyploid formation in PubMed DOI

Hunt HV, Ansell SW, Russell S, Schneider H, Vogel JC. Dynamics of polyploid formation and establishment in the allotetraploid rock fern PubMed DOI PMC

Koch MA, 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 PubMed

Zozomová-Lihová J, Krak K, Mandáková T, Shimizu KK, Španiel S, Vít P, et al. Multiple hybridization events in PubMed DOI PMC

Mavrodiev EV, Chester M, Suarez-Santiago VN, Visger CJ, Rodriguez R, Susanna A, et al. Multiple origins and chromosomal novelty in the allotetraploid PubMed DOI

Aellen P. Chenopodium In: Hegi G, editor. Illustrierte Flora von Mitteleuropa 3/2. München: Carl Hanser Verlag; 1960. pp. 569–659.

Chu GL, Mosyakin SL, Clemants SE. Chenopodiaceae In: Wu ZY, Raven PH, Hong DY, editors. Flora of China, vol. 5 Bejing and St. Louis: Science Press and Missouri Botanical Garden Press; 2003. pp. 351–414.

Kawatani T, Ohno T. Chromosome numbers of genus

Kawatani T, Ohno T. Chromosome numbers of genus

Giusti L. El gunero

Keener CS. Documented plant chromosome numbers 70:1. SIDA. 1970; 3: 533–536.

Uotila P. Chromosome counts on the

Uotila P. Chromosome counts on

Palomino GH, Segura M, Bye R, Mercado PR. Cytogenetic distinction between

Lomonosova MN, Krasnikov AA. Chromosome numbers in some species of genus

Lomonosova MN, Krasnikov AA. Chromosome numbers of the genus

Lomonosova MN, Krasnikov AA, Krasnikova SA. Chromosome numbers of the Chenopodiaceae species from Siberia. Bot Zhurn. 2001; 86: 145–146.

Bhargava A, Shukla S, Ohri D. Karyotypic studies on some cultivated and wild species of

Grozeva N, Stoeva M. Reports 1466–1472. In: Kamari G, Blanché C, Garbari F, editors. Mediterranean chromosome number reports– 16. Flora Mediterranea 16: 400–408.

Štorchová H, Drabešová J, Cháb D, Kolář J, Jellen EN. The introns in FLOWERING LOCUS T-LIKE (FTL) genes are useful markers for tracking paternity in tetraploid

Walsh BM, Adhikary D, Maughan PJ, Emshwiller E, Jellen EN. PubMed DOI

Dvořák F. Study of

Dvořák F. Study of

Dvořák F. Study of

Dvořák F. Relationships and diagnostic characters of

Dvořák F. Study of some species subsumed under

Jüttersonke B, Arlt K. Experimentelle Untersuchungen über die infraspezifische Struktur von

Uotila P.

Uotila P.

Vít P, Krak K, Trávníček P, Douda J, Lomonosova MN, Mandák B. Genome size stability across Eurasian

Gangopadhyay G, Das S, Mukherjee KK. Speciation in

Rahiminejad MR, Gornall RJ. Flavonoid evidence of allopolyploidy in the

Fuentes-Bazan S, Mansion G, Borsch T. Towards a species level tree of the globally diverse genus PubMed DOI

Fuentes-Bazan S, Uotila P, Borsch T. A novel phylogeny-based generic classification for

Štorchová H, Hrdličková R, Chrtek J, Tetera M, Fitze D, Fehrer J. An improved method for DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon. 2000; 49: 79–84.

Shaw J, Lickey E, Schilling E, Small R. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in Angiosperms: the tortoise and the hare III. Am J Bot. 2007; 94: 275–288. 10.3732/ajb.94.3.275 PubMed DOI

White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics In: Innis M, Gelfand D, Sninsky J, White T, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press; 1990. pp 315–322.

Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleid Acids Res. 2005; 33: 511–518. PubMed PMC

Sela I, Ashkenazy H, Katoh K, Pupko T. GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res.; 2015; W7–W14.; 10.1093/nar/gkq443 PubMed DOI PMC

Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symp ser (Oxf). 1999; 41: 95–98.

Ingvarsson PK, Ribstein S, Taylor DR. Molecular evolution of insertions and deletion in the chloroplast genome of PubMed

Simmons MP, Ochoterena H. Gaps as characters in sequence-based phylogenetic analyses. Syst Biol. 2000; 49: 369–381. PubMed

Müller K. SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Appl Bioinformatics. 2005; 4: 65–69. PubMed

Swofford D. PAUP* Phylogenetic analysis using parsimony (*and other methods). Version 4 Sunderland: Sinauer; 2002.

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19: 1572–1574. PubMed

Nylander J. MrModeltest v2 Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University; 2004.

Clement M, Posada D, Crandall K. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000; 9: 1657–1659. PubMed

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol. 2011; 28: 2731–2739. 10.1093/molbev/msr121 PubMed DOI PMC

Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies, Mol Biol Evol. 2006; 23: 254–267. PubMed

Zhong XB, De Jong JH, Zabel P. Preparation of tomato meiotic pachytene and mitotic metaphase chromosomes suitable for fluorescence in situ hybridization (FISH). Chromosome Res. 1996; 4: 24–28. PubMed

Lysák MA, Fransz PF, Ali HB, Schubert I. Chromosome painting in PubMed

Pijnacker LP, Ferwerda MA. Giemsa C-banding of potato chromosomes. Can J Genet Cytol. 1984; 26: 415–419.

Belyayev A, Raskina O, Nevo E. Chromosomal distribution of reverse transcriptase-containing retroelements in two PubMed

Mandák B, Krak K, Vít P, Pavlíková Z, Lomonosova MN, Habibi F, Douda J. How genome size variation is linked with evolution within

Heslop-Harrison JS, Schwarzacher T. Genomic Southern and In Situ hybridization for plant genome analysis In: Januhar PP, editor. Methods of genome analysis in plants. Boca Raton: CRC Press; 1996. Pp. 163–179.

Belyayev A, Raskina O, Korol A, Nevo E. Coevolution of A and B-genomes in allotetraploid PubMed

Kolano B, Gardunia BW, Michalska M, Bonifacio A, Fairbanks D, Maughan PJ, et al. Chromosomal localization of two novel repetitive sequences isolated from the PubMed DOI

Elder JF, Turner BJ. Concerted evolution of repetitive DNA sequences in eucaryotes. Quarterly Review of Biol. 1995; 70: 297–320. PubMed

Álvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol. 2003; 29: 417–434. PubMed

Kovařík A, Pires JC, Leitch AR, Lim KY, Sherwood AM, Matyášek R, et al. Rapid concerted evolution of nuclear ribosomal DNA in two PubMed PMC

Malinská H, Tate JA, Matyášek R, Leitch AR, Soltis DE, Soltis PS, et al. Similar patterns of rDNA evolution in synthetic and recently formed natural populations of PubMed DOI PMC

Tang L, Tang JM, Tan S, Li J, Ma X, Zhou ZQ. ITS sequence variation and concerted evolution in the natural hybrid species

Queiroz CD, Batista FRD, de Oliveira LO. Evolution of the 5.8S nrDNA gene and internal transcribed spacers in PubMed DOI

Ramsey J, Schemske DW. Pathways, mechanisms and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst. 1998; 29: 467–501.

Ramsey J. Unreduced gametes and neopolyploids in natural populations of PubMed

Mason AS, Pires JC. Unreduced gametes: Meiotic mishap or evolutionary mechanism? Trends Genet. 2014; 31: 5–10. 10.1016/j.tig.2014.09.011 PubMed DOI

Uotila P. Variation, distribution and taxonomy of

Hodač L, Scheben AM, Hojsgaard D, Paun O, Hӧrandl E. ITS polymorphism shed light on hybrid evolution in apomictic plants: a case study on the PubMed PMC

Fuertes Aguilar J, Rossello JA, Nieto Feliner G. Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of PubMed

Franzke A, Mummenhoff K. Recent hybrid speciation in

Zozomova-Lihová J, Mandáková T, Kovaříková A, Muhlhausen A, Mummenhoff K, Lysák MA. When fathers are instant losers: homogenization of rDNA loci in recently formed PubMed DOI

Kovařík A, Lim KY, Dadejová M, Matyášek R, Chase M, Knapp S, et al. Evolution of rDNA in PubMed DOI PMC

A pangenome reveals LTR repeat dynamics as a major driver of genome evolution in Chenopodium

Distinct hormonal and morphological control of dormancy and germination in Chenopodium album dimorphic seeds

Chromosome-Scale Genome Assembly of the Hexaploid Taiwanese Goosefoot "Djulis" (Chenopodium formosanum)